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Tuatara aims to stimulate and widen interest in the natural sciences in New Zealand, by publishing articles which (a), review recent advances of broad interest; or (b), give clear, illustrated, and readily understood keys to the identification of New Zealand plants and animals; or (c), relate New Zealand biological problems to a broader Pacific or Southern Hemisphere context. Authors are asked to explain any special terminology required by their topic. Address for contributions: Editor of Tuatara, c/o. Victoria University of Wellington, Box 196, Wellington, New Zealand. Enquiries about subscriptions or advertising should be sent to: Business Manager of Tuatara, c/o. Victoria University of Wellington, Box 196, Wellington, New Zealand.
(This issue edited by
is the journal of the Biological Society, Victoria University of Wellington, New Zealand, and is published three times a year. Joint Editors:
Virginia or White-Tailed Deer were introduced to New Zealand shortly after the turn of the century. Considered excellent hunting in their native habitat of North America, they were introduced for the purposes of sport. Two liberations were successful, one on Stewart Island, the other on the western shores of Lake Wakatipu. and the deer have remained confined to these areas. Concern over the damage inflicted by these and by red deer (Cervus elaphus) led to the removal of protection in 1925.
Virginia deer are placed in the Order Artiodactyla, Family Cervidae. Simpson (1945) includes them in a sub family Odocoileinae Pocock, 1923, but this is not mentioned in Hall and Kelson (1959), who place Virginia deer, together with black-tailed deer, in the genus Dama Zimmerman, 1780. However, the International Commission on Zoological Nomenclature (China and Melville, 1959) invalidated Dama Zimmerman, declaring Odocoileus Rafinesque, 1832 the correct genus for Virginia deer.
Odocoileus virginianus was first described by Boddaert (1785). The specific name virginianus is derived from the State of Virginia (the type locality) where this deer was found early in American history. Thirty subspecies are recognised throughout the range of the species, which extends from Coiba Island, Panama (O. virginianus rothschildi) to eastern Canada (O. v. borealis) and British Columbia (O. v. ochrourus).
The Virginia deer is also called the white-tailed deer owing to the conspicuous white tail which it holds upright when fleeing from danger. In North America the name white-tailed deer appears to be the most popular common name whereas in New Zealand it is Virginia deer. Other common names used in the United States are red-deer, common deer and karjacow (Donne, 1924).
Like many deer species, Virginia deer appear, at first glance, larger than they actually are, especially when only a glimpse is caught through the trees. On closer examination they prove to be slight and somewhat smaller than red deer. Height at the shoulder is about 3ft.: females are usually smaller than males. Blair et al (1957) point out that size varies considerably. Weight ranges from 50 to 350lb, but the average for males is between 120 and 150lb while females usually weigh between 80 and 100lb.
The upper parts of the coat are brownish red to grey in summer (a brighter red than the summer coat of the red deer), and become greyer in winter. The under parts of the body are white, as are the lower surface of the tail, the chin and throat, an area around the muzzle, and a ring round the eyes. The young are spotted, white on a reddish background, the spots being lost between the ages of three and four months. In New Zealand the change from summer to winter colour usually takes place in March and April and the winter-to-summer change in August and September, but these dates may vary considerably. The tail is very conspicuous because of its length (12-18in.) and its white underside (Fig. 1).
In common with other members of the Cervidae, only male Virginia deer (bucks) carry antlers. The main beam curves forwards with times arising vertically from it, brow tines are absent, and other tines are generally unbranched. Good antlers reach a length of 23-29in. (Riney, 1955) and occasionally may have up to 16 points.
Virginia deer have well developed senses of sight and smell. Their eyesight is particularly well attuned to movement, in this respect being more acute than that of red deer, but they seldom discern stationary objects. Their hearing is acute and they become alert at any strange or sudden sound; they seem especially aware of metallic sounds. In contrast with red deer, Virginia bucks are not vocal during the rutting period. Like most other species of deer they emit few noises and even then usually only if alarmed, when they blow through their nostrils. Sometimes a fawn will give a quiet bleat. When in flight their running is interspersed with a series of graceful leaps.
Virginia deer range from northern South America through Mexico and the United States to southern Canada. There is evidence that previously they inhabited all of the United States except some of the more arid areas, but have disappeared from many parts of their former range (Blair et al., 1957).
There is a wild introduced herd in Finland and there are some feral Virginia deer in England. Apart from these and the New Zealand herds the authors do not know of any Virginia deer established outside their present native distribution.
Four Virginia deer (two males and two females) were liberated in the Takaka Valley, Nelson, in 1901. It is not known who was responsible for this liberation or where the animals were obtained. This liberation was not successful.
In 1905, Five mule deer (Odocoileus hermionus), a deer very similar in appearance to Virginia deer, were also acquired by Donne at this time. These animals reached New Zealand in good condition and were liberated at Runanga, Hawkes Bay (Donne, 1924). In 1915 these deer were reported by the Hawkes Bay Acclimatisation Society to be increasing in numbers, but since then nothing has been heard of them and the liberation appears to have failed.
The herd on Stewart Island became well established and in 1917 the Southland Acclimatisation Society reported that the herd had increased considerably. Press reports in 1919 stated that it was a ‘splendid herd’ and two licences to shoot Virginia deer were granted. At the present time the highest densities of Virginia deer on Stewart Island are found in the northern part of the island, close to the coastline.
The herd at Lake Wakatipu has remained largely confined to the Rees Valley. It is only recently that they have become established in the adjacent Dart Valley (Fig. 2).
Virginia deer inhabit forest, forest edges and bush along stream edges. They avoid very dense bush, especially if it is damp, and
As with other members of the Cervidae, the sexes remain separate during most of the year except during the rut. In New Zealand this usually starts at the beginning of May and reaches a peak by the middle of that month, i.e. about 25 days later than that normal for red deer. Just before the start of the rut the bucks travel freely. Unlike red deer stags. Virginia bucks neither ‘roar’ nor wallow during the rut. Females usually breed in their first year if they are in good condition.
Young are born in December and January after a gestation period of approximately seven months (204 days according to Asdell, 1946). In their native habitat Virginia deer usually give birth to twins; triplets are not uncommon and quintuplets have been recorded. However, twins are rarely recorded in New Zealand. (One twin foetus was recorded in the Dart Valley in 1963, and twins are occasionally seen on Stewart Island.) The frequency of multiple births appears to be a reflection of the suitability of the environment, and it has been considered that the present environment of the Virginia deer in New Zealand is not entirely suitable. This view is supported by their failure to extend their range and by the generally poor condition of Virginia deer in New Zealand. In the Dart and Rees Valleys Virginia deer fawns are dropped a little later than those of red deer, but on Stewart Island the time of birth may be spread over most of the year; the mild climate of Stewart Island when compared with that of the Dart and Rees Valleys has been given as a reason for this (Daniel, pers. comm.). Fawns require milk up to the age of three months, and stay with the mother for eight or nine months. The association is usually broken when the doe is ready to have her next fawn. The conspicuous tail of the Virginia deer is used by the doe as a guide for the fawn as they run through the forest. Bucks also raise the tail, exposing the white under side, when they run from danger.
Virginia deer are quick to learn and to profit from experience. They will circle when they run from dogs; often they will let a person, or dog, approach and pass before quietly moving away. They make and frequently use ‘runways’. Once used to man, they will tolerate his presence, and in their native habitat Virginia deer may be found in large numbers on the edges of some of the big cities (Hall and Kelson, 1959). At Paradise Station (Glenorchy, Lake Wakatipu, South Island. New Zealand) Virginia deer can be observed by tourists, grazing at the bush edges.
Virginia deer will readily take to water, especially if pressed by dogs, and have been seen to swim for more than an hour and a half in calm water (Schofield, unpublished ‘report’). Bucks have swum more than three miles during the rutting period.
The parasitology and diseases of Virginia deer have been the subject of extensive investigation in their native country (Deer Disease Symposium. 1962). The New Zealand herd is currently being studied along similar lines by one of the present authors (J.R.H.A.). Preliminary findings from the Lake Wakatipu herd show the presence of dog tapeworm (Taenia hydatigena) cysts on the liver and omentum, a nematode (Oesophagostomum venulosum) in the caecum, and six species of trichostrongylid nematodes in the fourth stomach. The deer that were examined were in remarkably poor condition. Samples of blood taken from these animals failed to show the presence of Brucella or Leptospira organisms (Daniel, pers. comm.). The louse (Damalinia parallela) commonly found on North American Virginia deer was also present.
In North America Virginia deer are host to a wide variety of parasites, including a number that are shared with other wild and domestic ungulates (Anderson, 1962).
Virginia deer were protected until 1919, when regulations were gazetted for shooting under licence. In 1925, as a result of representations made to the Government, all protection was removed. The number of Virginia deer shot either by Government hunters or by private shooters is not known. Extensive operations against both red and Virginia deer on Stewart Island reduced the numbers of the red deer, but Virginia deer, because of their more wary nature and their habit of occupying bush country, remained numerous.
Virginia deer have little commercial value. It is hoped that they may provide a tourist attraction in the Wakatipu (Glenorchy) area. Donne (1924) observes that Virginia venison is highly recommended because it is readily digested. The meat is lighter in colour than that of red deer, not as coarse, and can be very tender. Donne also quotes Theodore Roosevelt as stating that ‘Whitetail venison is most delicious eating’.
E. L. Hellaby Research Fellow.
An Earlier Account by Wardle (1963) presented an hypothesis of Pleistocene extinction of plants in the central South Island, and the likelihood of the presence of Pleistocene refugia in the extremities of the Island, among other places. The present writer, independently, had come to similar conclusions from study of distributions of species in the South Island. This paper was written in the belief that it could add considerable detail to the chain of evidence presented by Wardle and elucidate some of the problems of distribution.
Two groups of plants are disjunct For plant geographical terminology see Cain (1944). Readers are referred to A Descriptive Atlas of New Zealand for place names.
The second striking series of disjunct species consists of plants with a conspicuous gap in their known distribution in the central South Island. Wardle listed a few of these and drew on the presence of a relatively large number of endemic plants in each of Otago-Southland and Nelson-Marlborough, with correspondingly few endemics in the central South Island, as support for his hypothesis of Pleistocene extinction in the latter area. An implication of the hypothesis is that Nelson, Marlborough, Banks Peninsula, coastal Southland. Stewart Island and offshore islands were refugia where large numbers of species including some forest plants survived the glacial maxima of the Pleistocene.
In examining, the present distribution patterns of species disjunct between the northern and southern parts of the South Island, and of endemics in both these areas, the present writer came to the conclusion that a simple statement of Pleistocene extinction in the central South Island did not explain all the facts of distribution. The detailed knowledge of distribution of plants and vegetation, together with information from non-botanical fields, allows elaboration of the hypothesis as formulated by Wardle. In this article evidence is brought forward in support of a modified hypothesis.
It is proposed here to deal with species fully disjunct between Nelson-Marlborough (and/or North Island) and Otago-Southland (and/or Stewart Island); with closely related (vicarious) species, whose distributions do not meet in the central South Island; with species which are abundant to north and south of the South Island and less common between; with the patterns of distribution of species endemic to the north and south of the South Island; with some distributions which indicate that the populations of these plants have undergone recent contraction: and with some disjunct animal distributions.
The species fully disjunct between the northern South Island (and/or North Island) and southern South Island (and/or Stewart Island) in a few cases extend to the Auckland or Campbell Islands. The gap in distribution varies in width and is obvious from distribution maps (Figs. 1, 2, 3 and 4). The extremes in separation are those for populations of Juncus procerus (Edgar, 1964), 1650 miles, from Auckland to Southland) and for Drosera pygmaea, from the Volcanic Plateau to Bluff Hill (more than 600 miles). In the South Island proper there are patterns held in common by numbers of species. Many of the species are confined to the Gouland Downs-Tasman Mountains-Mt Arthur-Paparoa Range areas in the north and to Stewart Island-Fiordland-Longwood Range-Blue Mountains-Maungatua in the south. The ranges of other species are further to the south in Nelson-Marlborough and to the north in Otago-Southland with limits in various places, a few extending as far as Canterbury-Westland. One species ( Pimelea aridula)‡ is centred on Central Otago and central Marlborough, and lives on dry, rocky hillsides. It extends also to Hawkes Bay. The other full disjuncts include
There is a group of several pairs of morphologically similar species in which one of the pair is distributed in Otago-Southland and the other in Nelson-Marlborough or North Island. There is, thus, a gap in the central South Island in which the pairs of species do not meet. These pairs seem to be closely related or vicarious species. It may be speculated that they have experienced evolutionary divergence comparatively recently (probably following separation earlier than the disjunct species were separated). They are enumerated below.
The distribution patterns of a further group of species show that they are generally abundant in the north or south of the
Nothofagus menziesii occurs in the north west and south west and south of the South Island but is found in at least three scattered localities — near Burkes Pass, at Lake Heron and in the Karangarua Gorge, between the main areas of occurrence. The Armstrong herbarium of the Canterbury Museum contains two specimens of each of Nothofagus menziesii and N. fusca labelled as having been collected in the Upper Rangitata and Upper Ashburton Rivers in 1869 but these distributions require verification. Adenochilus gracilis nearly always accompanies Nothofagus fusca. There is one known occurrence of this orchid in the Whitcombe River, a tributary of the Hokitika River.
There are sufficient endemic vascular plant species in the South Island confined within the areas north of a line from about Greymouth to Motunau and the south of a line from about Bruce Bay to the Waitaki River mouth to enable the northern and southern floras to be regarded as distinct from the rest of the South Island flora (see Wardle, 1963a; approximately 110 endemic species in Nelson-Marlborough and 90 in Otago-Southland excluding the Foveaux Strait species). The central South Island proper, however, is characterised by relative poverty in endemic species, with only about 14 such species being confined approximately within the boundaries described above, four of them on Banks Peninsula. Some of these central South Island endemics are plants of rupestral habitats and others favour periglacial habitats up to about 9000 feet in the high Central Alps (Myosotis explanata, Ranunculus godleyanus, R. grahamii). Rupestral, scree and high altitude species of somewhat wider distribution will be discussed later. Individual distribution patterns of the endemics which have been grouped here into Nelson-Marlborough and Otago-Southland floras resolve the endemics into minor groups centred on focal areas within both northern and southern South Island. Thus there is a group centred on northwest Nelson and a smaller group in eastern Nelson, and Marlborough including the Kaikoura ranges. Similarly in the south a group centres on Fiordland and another on Central Otago. These may be designated ‘western’ and ‘eastern’ facies respectively, but individual species transgress any boundaries which may be drawn. The fully disjunct species and vicarious pairs of species have similar distributions. It is not intended to enumerate the distributions of these endemic species in detail. The generalised patterns of distribution will be described with the aid of a map (Fig. 7). From Fig. 7 it is seen that northern patterns may be grouped into at least nine ‘types’. These are designated only for convenience in description. Individual distribution patterns show great complexity, with each species tending to behave independently. Each ‘type’ is named here according to the absolute southern limit of the species within it and is characterised by the presence of at least three species.
Since this article was written further field work reveals that another group of southern species has its northern limit in the Haast Pass-Lake Ohau region. The species include Dracophyllum menziesii,
In all the patterns so far described the species involved are relatively abundant and continuously distributed within their area. Later in this account there are also recorded a few cases of species from northern and southern New Zealand which show considerable disjunction between continuous populations and other known localised occurrences. This is probably to be related to contraction of areas.
The general situation as expressed in Fig. 7 is that from several centres (which are probably centres of dispersal), species distributions radiate outwards. Common limits are reached by groups of species, but patterns tend to be different for each individual species. This is to be expected in view of the likely differences in tolerance ranges between different species. The patterns tend to be eccentric about the centres of dispersal. There are tendencies for species to be restricted towards west or east and this is reflected in the presence of ‘western’ and ‘eastern’ facies. but some of the species extend into both western and eastern areas. It seems clear that species have migrated outward
A further situation complicates the position with respect to the hypothesis of Pleistocene extinction in the central South Island. Outside the main areas of distribution of numbers of species there are found distant, isolated occurrences. The ‘partial’ disjuncts described previously are of this type, but many others also exist which are not dicentric. Again, in these monocentric patterns the tendency is for a distribution to tail-off into the central South Island. The gaps between populations seem too great to have been bridged by long distance dispersal. In most cases, too, the apparent lines of dispersal lie athwart prevailing wind gradients or likely pathways such as river valleys and mountain ranges. Contractions of area are believed to be the explanation for these distributions. Species which appear to have contracted northward are: Celmisia allanii, continuous to the Hurunui River, one occurrence in the Godley River: Hebe cheesemanii, continuous to Hurunui River, occurrences at Mt Peel, South Canterbury, Kirkliston Range and Mt Alta, Otago; Ranunuculus insignis (‘monroi’ type), continuous to Waimakariri River; occurrences at Mt Hutt, Mt Peel and Four Peaks; Leucogenes leontopodium, local but not uncommon on North Island and Wairau Mountains, isolated populations at Hurunui River and Mt Peel; Hoheria sexstylosa, common to about 40 deg. 30 min. south latitude, occurrences on Banks Peninsula (possibly now extinct) and near Gore;
It seems probable that these monocentric and some or all of the ‘partially disjunct’ dicentrically distributed species have undergone contraction later than the separation of the species regarded as full disjuncts. Some of the latter may also have had their areas contracted.
Some animal distribution patterns fit into the general patterns of plant distributions outlined above. Powell (1957) described the following marine animals with disjunctions in their distributions between North Island and South Island: the mollusc Amphidesma ventricosum (toheroa) and at least one other mollusc and a species of brachiopod. Fleming (1950) described a molluscan fauna from the coast of Fiordland containing three genera and 16 species otherwise known only from North Auckland or North Island. Mr P. Johns (pers. comm.) states that although there are no species known by him to be disjunct between Nelson-Marlborough and Otago-Southland, certain groups of species of the terrestrial animals, ground beetles, millipedes and cockroaches are closely related in the two areas, separated by a gap in the central South Island. They are probably equivalent to the pairs of vicarious plant species. Similarly, the distributions of individual species extending into Canterbury from north and south are parallel in many cases to plant distributions. Lee (1956, 1959) recorded that one genus of earthworms in New Zealand was represented only in Fiordland and Auckland Province, and three species of Taranaki-Wanganui are most closely related to species of the south-western South Island and subantarctic islands. Comparatively unspecialised faunas consisting of widespread species are present in the eastern South Island. Westland is likewise unspecialised with respect to earthworms but there are some endemic species and the area had been colonised from both north and south. Banks Peninsula is also an area with a small number of endemic earthworms. The Wellington-Nelson area is regarded as a centre of dispersal for these animals.
Distributions of many plants and some animal groups suggest that there is a real floristic-faunistic gap in the central South
A brief consideration will now be made of the role of glaciation and post-glacial climatic changes in bringing about discontinuous distributions. A more detailed account of these changes, together with interpretations of the available pollen analyses will be published elsewhere. References for the statements made below are included in Burrows (1964 M.S.).
The last major glaciation, known as the Otira Glaciation (Gage 1961), was preceded by an interglacial in which there is evidence for mild climates and vegetation similar to the present in the South Island. This probably is the time when most of the plant species now disjunct were distributed throughout the Island. The onset of the first stadial of the Otira Glaciation brought about their disjunction. The vicarious pairs of species may have evolved after disjunction brought about by one of the earlier Pleistocene glaciations. Even at the height of each stadial some vegetation would have survived throughout the South Island. This would have included scrub and tall and short tussock grassland composed of unspecialised species now widely distributed. Specialised species of scree, rock and ‘periglacial’ sites would also have been present in the many suitable habitats. Many other species including forest trees would have been limited by cold to refugia in extremities of the island. During the interstadials before the last (Blackwater 2 and Poulter) ice advances of the Otira Glaciation (Gage and Suggate 1958) forest species including B.P — before 1950 A.DNothofagus s. cliffortioides and N. menziesii expanded into the central South Island (as they probably did during each interstadial, to be pushed back as the next ice advance began). This vegetation was probably not completely dislodged from the centre of the Island by the subsequent ice advances. It was, however, likely to have been severely limited. Soon after the retreat of Poulter ice about 15,000 years B.P.Phyllocladus alpinus, Dacrydium biforme) and the larger
Podocarpus hallii, with scrub and grassland existed east of the main divide in the centre of the island proper. In central Westland the vegetation was much as it is at present, although podocarp stands on the young surfaces were probably denser. It is likely that the alpine species with present restricted distribution began to recolonise the central South Island from the northern and southern refugia contemporaneously with the lowland species. Many other more widespread alpine species would have been drawn from the flora of grassland vegetation which occupied the lowlands during glacial maxima. They would have occupied various open habitats during the reforestation of deglaciated areas. In the light of this early reforestation, the failure by some species to complete the colonisation of the central South Island is puzzling.
The explanation of this apparent anomaly is thought to be two subsequent events. The first of these was a renewed ice advance, less extreme than the Poulter advance. By analogy with events in the northern hemisphere and in South America (Flint 1961, Auer 1956, 1958) this short-period stadial, known in New Zealand as the Birch Hill advance, occurred about 10,000-11,000 B.P. The moraines left by it are most evident in the central South Island, and there were probably only cirque glaciers in Nelson and Fiordland. Soon after the Birch Hill ice advance there began a period of cool (upland) to warm (lowland) moist climate known as the ‘climatic optimum’. This effectively prevented further beech advance at the time. Cranwell and von Post (1936) and others have demonstrated how podocarp-broadleaved forest during this time largely superseded beech forest. Beech was, however, present at all times and must have been restricted to higher altitudes and various somewhat extreme habitats. At the fronts with mixed forest in central Westland, the Taramakau and Paringa Rivers, beech species remain limited to the present day by efficient competition chiefly from broadleaved trees such as Quintinia acutifolia and
Some of the discontinuities in populations of ‘partial disjuncts’ and monocentric species which have undergone contraction may have been brought about by the same causes. It is difficult to conceive of any phenomenon so profound that it could cause extinction in the central South Island on the scale described in the opening part of this article later than the last main series of glacial advances of the Pleistocene. The Birch Hill and later advances do not seem to have been intense enough to cause primary disjunction. It seems probable however that post-Poulter climatic changes have inhibited plant migrations from refugia and have also in more recent times brought about contractions in areas. It is probable that subsequent to the period of moist climate with mild temperatures between about 9,000 B.P. and 5,000 B.P. (for dating see Deevy and Flint, 1957) climates began to become at first warmer and then increasingly cooler and drier. Some specific data on distributions of certain plant species support this theory of climatic deterioration probably since about 2,500 B.P. A peat sample from the Grey River valley dated at about 8,300 B.P. (Bowen, ex Grant Taylor and Rafter, 1962) contained Metrosideros robusta pollen (a little south of its present range) and a small amount of Agathis australis (Dr
Scattered discontinuous distributions of various other widespread species throughout the South Island may have resulted from the same causes of contraction as the examples described above. One cause of many such discontinuities in the eastern South Island, however, undoubtedly is fire during the Maori era (see e.g. Molloy et al. 1963). Subfossil remains demonstrate that forest has been extensively fragmented by fire within the last thousand years. Species dependent on a forest environment are limited by this (see Burrows 1961). Fire is not the only likely cause of discontinuity, nor even the primary one since the evidence for climatic deterioration in the last few thousand years is quite clear. Climatic fluctuations seem to have continued up to the present (Holloway 1954, Wardle 1963b).
Brief consideration of the Auckland-Nelson disjunction (Wardle 1963a) may now be made. During the early Otira Glaciation the southern and central North Island apparently were subjected to severer climatic conditions than was north-west Nelson. The latter area was at the western side of an extensive plain exposed by low sea levels (Fleming 1962). General extinction of forest occurred in the southern half of the North Island although scrub and grassland were present at lower altitudes. During the Poulter stadial beech forest was probably extensive. The question as to whether the tender kauri associate species survived the whole Otira Glaciation in north-west Nelson is still an open one. The influences of Birch Hill cooling have not yet been recognised in this area nor in the North Island. The ‘climatic optimum’ climates would have enabled expansion southward of the kauri associates (and probably kauri itself) so that disjunction of these species may be subsequent to it. Vulcanism in the central North Island (see e.g. Taylor 1953) is almost certainly an important contributor to limitation of many species north of the 38th parallel. Widespread ash showers have probably been as efficient in causing extinction in the centre of the North Island as glaciation in the centre of the South Island, but their invocation as a cause of complete extinction in the whole southern North Island poses various problems. Why did some of the species concerned not survive in the western North Island or near Wellington?
The detailed information presented above supports the general hypothesis of Wardle (1963a) that the Pleistocene glaciation caused extinctions of plants (and animals) in the central South Island and contractions into refugia. In the north, the refugia are likely to have been the coastline and hills of north-west Nelson to the Paparoa range, the coastline of Marlborough and, by virtue of a few plants endemic there, Banks Peninsula. In the south, refugia
As a result of this detailed knowledge of distribution some doubt is cast on the validity of the botanical district concept as framed by Cockayne (1928). On the basis of numbers of endemic species three main floristic areas may be discerned in the South Island (Fig. 8). Each of these contains at least 80 endemic angiosperms. They are: 1. Nelson-Marlborough. 2. Otago-Southland-Stewart Island, 3. An area which overlaps with both of these and runs the length of the island along the mountain chains from Nelson to Southland. There is a concentration of endemics in this latter area mainly east of the main divide and many of
Grateful acknowledgment is made for permission to consult specimens from those responsible for the herbaria of the Canterbury Museum and the Botany Division, D.S.I.R. I have also to thank Mr Pimelea aridula. Several of my colleagues have offered useful criticisms of the script and I express my thanks to them. I am especially grateful to Dr
InTuatara 12 (3): 155-6, 1964, Trichosurus vulpecula. At first glance this situation may seem inconsequential because no ambiguity is possible if the scientific name is also given. But ‘vernacular’ names of birds and mammals usually have a greater stability than scientific names, and are used by zoologists to a considerable extent. I have placed ‘vernacular’ in quotes because the word implies that a common name is coined by some mead-drinking peasant in the murky past, and arises entirely uncontaminated by scientific research. This might have been true a century ago, but people now identify an animal by referring to books on the subject, most of which are written by zoologists. Zoologists have thus become the originators and arbiters of both scientific and common names. This is inevitable because many birds and mammals have either no true vernacular name or share a name with several other species.
A glance through the scientific papers published on Trichosurus in the last ten years shows that most zoologists (and all Australian zoologists) have used ‘possum’. The reason for this preference is obvious: to use ‘opossum’ for Trichosurus confuses it with Didelphis, and these two genera are as far apart taxonomically as are mice and elephants. ‘Possum’ is common usage in Australia. Mr Kean did not indicate which name he favoured for use in New Zealand but I suggest we conform to international usage. This would standardise the common name and remove the anomaly of two distinct animals sharing one name. In addition, I will be relieved of the embarrassing responsibility of explaining to overseas visitors that we do not have Didelphis in New Zealand (this has happened three times so far) despite what they may have read on the occurrence of the ‘opossum’ in this country.
These views are my own and are not necessarily those of my department.
In this and a following article the New Zealand species of two liverwort genera of importance in elementary teaching are described. The present article considers Lunularia cruciata, and it is suggested that as this species is much more common than the standard textbook example Marchantia, greater use could be made of it in teaching.
In the second article the three species of Marchantia occurring in New Zealand will be described and details given of their occurrence and reproductive cycles.
The Liverwort GenusLunularia has only one species, L. cruciata (L.) Dum. (Stephani, 1900). It belongs to the Marchantiales and, although showing an intriguing resemblance to Marchantia in its type of gemma, it is in many respects less specialised and is sometimes placed in a family of its own (Hassel de Menendez, 1962).
Although Lunularia was first described from Europe by Micheli in 1729, it is now known to be widely distributed (Frye and Clark, 1937). In many countries it is adventive, for it occurs in greenhouses and in the shaded parts of gardens. Watson (1959) remarks that it is perhaps not a true native of Britain, as it is rare away from habitations. Smith (1955) considers that it was introduced from Europe to U.S.A. with nursery stock and states that, although widely spread in greenhouses throughout the country, only in areas with a mild climate such as California has it become established outdoors.
Lunularia as described in the literature is morphologically uniform throughout its range except in South America. Here, along with forms differing in no respect from those in Europe, there occurs in Chile, Peru and Argentina a type in which the walls of the dorsal epidermal cells are greatly thickened and the ventral surface of the thallus is coloured dark purple. Although this type has been described as a separate species (Herzog, 1938), Hassel de Menendez by maintaining plants in cultivation has shown that the distinctive features become less pronounced. Also at the margin of its range she found plants of intermediate character (Hassel de Menendez, 1962). She considers there is justification for recognition of a form only and names it forma thaxteri (Evans and Herzog) Hassel de Menendez. Writers frequently remark on the fact that sporophytes are very rare. They have been found once at Cape Town (Saxton, 1930), at San Diego, California (Frye and Clark, 1937), at a few places in southwest England
In New Zealand A further finding of both well-developed and mature sporophytes was made at Rangitoto Island in mid-February 1965, and of sporophytes with dehisced capsules by G. A. M. Scott at Dunedin in early February, 1965.Lunularia is abundant at the present time. However, Hooker (1867) makes no mention of its occurrence and, as it seems unlikely that a plant so well-known in Europe would have been overlooked by early collectors, it may be assumed that it has been introduced to this country. It occurs as a troublesome weed of greenhouses and shaded gardens but is also well established as a wild plant amongst native shrub vegetation, in some cases in isolated areas at a distance of up to 20 miles from the nearest farm homestead. Most flourishing colonies were found to form archegonia or antheridia. Sporophytes, however, are not often seen,thaxteri.
The thallus of Lunularia is normally green to yellowish-green in colour, but with age it turns brown, either at the edges or all over. Up to 4 cm, or rarely to 7 cm long, and up to 1 cm, or rarely to 1.8 cm wide, it grows flat on the ground or over existing thalli, often forming extensive colonies as it spreads.
Branching occurs by bifurcation of the apex and, when the latter ceases activity, regenerative growth occurs from adventitious shoots. Above, the thallus often appears somewhat glossy and under a lens can be seen to be marked out into polygonal areas each with a
u in diameter which grow vertically downwards, and narrower, tuberculate ones, 7-24 u in diameter, which near the thallus lie horizontally in bundles and distribute the available water evenly over the lower surface.
On the upper surface of some thalli are groups of disc-shaped gemmae lying in a cupule on the mid-line and protected on the posterior side by a crescent-shaped ridge with a crenate, or in old thalli an almost entire margin (Fig. 1). Each gemma has 2 opposite, lateral growing-points (Fig. 5) and is at first attached by a short stalk, but when mature it becomes detached, floats away in water and under favourable conditions grows into a new plant (Fig. 6). The crescentic cupules containing the gemmae are distinctive of the genus and are responsible for its name.
In structure the thallus shows considerable organisation. In the central portion it is 0.5-1.0 mm in depth and gradually becomes thinner towards the margin. The dorsal epidermis consists of colourless or almost colourless cells; sometimes the walls are thin but often those of centrally placed cells have triangular thickenings known as trigones at the angles and in plants from the open all the walls may be evenly thickened, this being particularly noticeable when the thallus is fresh (Fig. 4). Below the epidermis is the photosynthetic tissue consisting of a single layer of air-chambers separated by green, uniseriate partitions and occupied by numerous, erect, green filaments 3-5 cells high. The air-pores leading into the chambers are elevated above the surface of the thallus (Fig. 2) and are simple in structure, not barrel-shaped as in Marchantia. The compact, ventral tissue is 18-35 cells deep in the midrib region but gradually becomes thinner towards the wings; it is a storage region composed mainly of colourless cells with pitted walls, but scattered cells contain brown oil bodies, and septate fungal hyphae similar to those reported from Lunularia in South Africa (Auret, 1930) may be present in a zone of the midrib region. Fungal infection is sporadic and plays an insignificant role in the life of the plant as has been noted in other countries (Ridler, 1923; Auret, 1930; Nicolas, 1924, 1932). In plants growing in
Marchantia-type initial cells situated at the base of the apical cavity. Although in vertical sections of the vegetative thallus a single wedge-shaped initial cell is apparent, in horizontal sections two similar rectangular cells are usually recognisable, as recorded also for Marchantia planiloba (Burgeff, 1943).
In regard to sexual reproduction Lunularia is dioecious. The antheridial receptacle is a slightly elevated, flat disc 3-4 mm in diameter surrounded by a circular, membranous, cupule-like sheath with a crenate edge (Fig. 1). Originally terminal on one branch of a dichotomy and alternating as to the side of occurrence on the plant, it soon becomes left behind by the onward growth of the thallus and appears to be situated in a lateral position. The antheridia (Fig. 9) are individually sunken in flask-shaped cavities opening to the surface by a simple pore at the end of a canal. In old receptacles the cells adjoining the cavity and the canal tend to turn reddish-purple. Young receptacles were forming in sheltered situations from May until the end of September, at which time most male thalli undergo regenerative growth and produce cupules. Development of the antheridium (Figs. 7 and 8) was found to follow the pattern shown by other members of the Marchantiales, as indeed Saxton (1930) implies, although other interpretations have been given (Chalaud, 1931). The sperm cells are exuded from the mature ovate antheridium in an opaque mucilaginous mass and lie on top of the disc until wetted, when the spermatozoids become free-swimming. Such masses of sperm cells are readily found on plants in the greenhouse and out-of-doors near Palmerston North from mid-July until September. Under conditions of water deficit, however, the antheridia are halted at various stages in development and remain in situ for many months.
The archegoniophore also develops in a terminal position on one branch of a dichotomy but sometimes owing to continued growth of the vegetative branch it becomes left behind in an apparently lateral position. It alternates as to the side of occurrence on the thallus and makes its appearance from May until September with different populations varying as to the starting time. The archegoniophore lies centrally on the floor of a shallow, circular cupule with a crenate rim. For a long time it remains as a
Marchantia species are not present. Development of the archegonium occurs as in other members of the Marchantiales and the mature archegonium is typical of this group (Fig. 10).
Fertilisation takes place readily when spermatozoids are transferred in water by means of a pipette, and on occasions so abundantly that some developing embryos are suppressed. It occurs less readily by natural means both in the greenhouse and out-of-doors near Palmerston North.
The general development of the sporophytes has been described by Saxton (1930). However, from the abundant material available it is possible to add some supplementary notes regarding the early stages. The fertilised egg remains dormant for a period of 4 to 6 weeks though recognisable by its slight increase in size and its denser cytoplasm. Meanwhile both the enclosing calyptra and the archegoniophore are enlarging and accumulating much lipid and protein material. Then suddenly the embryo commences active growth while both the calyptra and the archegoniophore continue their enlargement. The first division in the embryo is transverse (Fig. 11), and this is followed by another transverse division in the upper cell so giving a file of 3 cells (Fig. 12), which by further development produce the foot, the seta and the capsule respectively (Fig. 16). In the foot region a vertical division is followed by further growth and by divisions in various planes until there is produced a massive structure which penetrates through the base of the archegonium into the tissue of the archegoniophore. The seta initial cell divides first by two intersecting vertical walls and then a few times in other planes but active growth and division in this region occurs only when the sporophyte is almost mature. In the capsule region the course of development, as pointed out by Saxton (1930), is of an unusual type. Two intersecting vertical walls give 4 cells each of which now divides transversely (Figs. 13 and 14). The formation of periclinal walls cuts off jacket cells from central cells (Fig. 15). Most of the capsule wall is derived from the jacket cells but the extra layers of the cap region are derived from the upper tier of the central cells. The lower tier of central cells cuts off
When the sporophytes are nearly mature, the stalk of the archegoniophore elongates in just a fortnight to a height of up to 22 mm, so lifting the disc well above the ring of scales (Figs. 3 and 21). At this stage the whole archegoniophore is conspicuous by its general appearance of whiteness, although on close inspection the green foot of the sporophytes is visible within its tissue. The stalk has no rhizoid-furrow and no photosynthetic tissue. It is 1.0 mm in diameter and is more or less shaggy with scattered,
The mature-sporophyte consists of a small green foot, a colourless seta (stalk), and a dark-brown capsule which contains spores together with elaters. It develops within a calyptra and until almost mature is enclosed by the thin involucre. Then on a dry day the involucre unfolds distally to become bilabiate and the seta, which recently has been dividing actively, elongates rapidly to a length of 3 mm, so pushing the capsule beyond the opening (Fig. 3). In several instances there were 2 sporophytes within the one involucre, as was noted also in material from southern England (Saxton, 1930). The capsule is oval in shape and 1 mm long; its wall lacks annular thickenings and is made up of one layer of brown-walled cells except at the top where there is a minute cap 2-3 cells deep of a darker-brown colour (Fig. 17). The ripe capsule opens lengthwise to the base into 4 valves which sometimes begin to divide again lengthwise, but the tiny cap is shed intact. The spores are tetrahedral with a faint tri-radiate marking on the otherwise smooth wall; in colour they are a pale greenish-yellow and in size rather variable with a diameter ranging from 9 to 16 u. The elaters are bispiral, of width up to 10 u and of length 300-430 u, tapering at the ends to a long point. Once the spores are shed the fragile archegoniophore soon collapses.
In order to investigate the germination of the spores these were scattered either on inverted flower-pots filled with sphagnum moss and watered from below with Knop's solution, or in petri dishes on Knop's solution in agar surface-wetted with distilled water. Germination occurs in 10 to 20 days, this being longer than the time given by Chalaud (1932) perhaps due to the fact that the spores dissected from the capsules were not quite mature.
When the spores are well spaced out and the dishes are kept in the light, the course of germination was found to be as follows. The spore enlarges to twice its original diameter and opens in the region of the tri-radiate marking. A colourless rhizoid emerges and is cut off by a wall. The green cell grows rapidly and breaks out of the fragmenting spore coat, dividing first by a more or less vertical wall (Fig. 18), and then each resulting cell dividing both transversely and vertically in a plane at right angles to that of the first division, so giving an octant stage. The sporeling is now approximately spherical in shape but soon becomes irregular when an apical cell arises in one or other of the octants and begins to divide actively (Fig. 20). The apical cell has four faces in contact with neighbouring cells (Fig.
Lunularia as found in New Zealand corresponds with plants described from other countries. Transplant experiments indicate that in New Zealand the form with thin walls in the dorsal epidermis is a shade form developing under glass in greenhouses and in continuous shade outdoors. The form with trigones on the epidermal cells develops under better lighting, either in the open or in hardening-off frames. The form with much-thickened walls is found less commonly, for its requirements of comparatively high light-intensity together with coolness and high humidity are rarely
Whereas some colonies near Palmerston North produce sporophytes freely, not all do so. Several reasons can be given to account for their absence. Firstly, some colonies consist of sexually immature or juvenile plants with a thin thallus and scanty food-reserves, for in many instances Lunularia behaves as an opportunist spreading rapidly by vegetative means on disturbed soil, on rock or on brickwork before the arrival of other species. Gemmalings are in this juvenile state for over a year, for even under favourable conditions those formed in autumn and winter do not become sexually mature until the winter or spring of the following year. When plants are damaged by dryness of the air or by extremes of temperature or are disturbed by management practices, re-establishment may occur from gemmae previously lodged amongst the rhizoids or in folds of the thallus, or from adventitious juvenile shoots developing on any still living remnants of the original thallus. Under natural conditions near Palmerston North these latter develop abundantly in late spring and to some extent in autumn. Continued repetition of the regeneration process may produce a colony in which the juvenile state is perpetually maintained.
Secondly, the development of antheridia and archegonia is not always synchronised. Female thalli in late autumn, even when green and fleshy and bearing sporophytes, do not continue apical growth but regenerate from approximately 3 strongly-growing adventitious thalli which, after producing cupules, being to produce archegoniophores at various times from May until September. Even when plants are grown alongside one another in the greenhouse, different populations vary as to when they start to form archegoniophores; and in the open the growth in almost all populations is liable to be checked at any time by unfavourable weather. Male plants behave differently as, even when dried out, they often grow again from the resistant apex once the rains commence in late autumn. New antheridiophores arise and old ones revive and continue development but as with the female plants growth may be halted at any time by unfavourable weather. Where, however, the male plants die off in autumn and regenerative growth occurs, the new thalli at first resemble gemmalings and grow very slowly; only in the greenhouse were they sufficiently advanced to form antheridiophores late in the season. In the open they develop so slowly as compared with female plants that the population under these conditions appears to consist solely of female plants. Populations entirely or predominantly of female plants have been noted also in other
Provided sexually mature male and female plants are growing intermixed, fertilisation was found to occur quite readily. However, the sporophyte takes several months to mature and, since its delicate coverings are inadequate for protection from drying winds, few survive to maturity. In an unheated propagating pit in the greenhouse the sporophytes developed satisfactorily.
Recent experimental work with the Israeli strain of Lunularia has demonstrated a response to photoperiod (Nachmony-Bascomb and Schwabe, 1963; Schwabe and Nachmony-Bascomb, 1963; Wilson and Schwabe, 1964). However, any interpretation of the behaviour of the New Zealand plants in the light of these findings is complicated by the fact that winter temperatures in New Zealand are much lower than any used in the experimental work.
In the caption beneath the photograph of Squilla armata in Tuatara, Vol. 12, No. 3, p. 185, it was stated that this species is fairly common in New Zealand and southern Australia. The latter locality is incorrect. Records of Squilla armata from southern Australia refer to another species.
In Part I of this article (Tuatara Vol. 12/2) I attempted to review in some detail the structure of the cell nucleus and to briefly indicate the importance of the nucleus to the cell as a working, integrated unit. This second part of the article describes the cell nucleus and the cell as a whole in division. I have tried to picture cell division as a dynamic process with many facets that interact to produce the whole. Thus I have given some detailed attention to a causal analysis of what appear to be the most important phenomena of cell division, rather than confining the article to a redescription of the well known (though often poorly understood) elements of the process. It is unfortunate that nearly all text books treat the subject as if it were completely understood, or emphasize certain hypotheses to the exclusion of others and factual evidence, so as to present the picture that these hypotheses are virtually factual. For this reason I have tried to differentiate clearly between fact and hypothesis; what is understood and what is not; and to create in the reader an attitude of enquiry. I have also tried to indicate the intimate relationship between mitosis, meiosis, fertilization and heredity.
Two distinct phases of cell division are distinguishable, karyokinesis (nuclear division) and cytokinesis (cytoplasmic division), and when cells divide these two processes generally go hand in hand in nearly all tissues, with cytokinesis geared in time and place to the closing phases of karyokinesis. Karyokinesis is referred to as mitosis. The term mitosis comes from the Greek mitos meaning a thread, and -osis indicating a process, and mitosis literally means a process (of division) involving thread like bodies. These thread like bodies we call chromosomes, discrete rod shaped structures that represent the state of the nuclear chromatin during the visible phases of nuclear division. The drama of mitosis does in fact centre round the chromosomes but we shall see that it involves much more than just the chromosomes, or even just the nucleus; the cytoplasm also undergoes important changes during mitosis, changes without which nuclear division could not possibly be achieved. As with all aspects of the workings of cells, mitosis involves the cell as a unit.
Two types of mitosis are associable with cell division, somatic and meiotic. Somatic mitosis (usually referred to simply as mitosis), coupled with cytokinesis, gives rise to new body (soma)
meio, to lessen) is a special type of nuclear division associated with the formation of gametes in male and female sexual reproductive organs; it is, in essence, a reduction division, giving the haploid number and set of chromosomes to each cell produced and so counteracts the doubling of the chromosomes at fertilization. Meiosis also permits the reshuffling of genes between homologous chromosomes and so paves the way for character variation in different individuals of a species.
Mitosis is a continuous dynamic process but for descriptive purposes it is convenient to divide it into five phases; prophase, prometaphase, metaphase, anaphase and telophase. Prophase begins from an interphase-metabolic nucleus that has been undergoing preparations for division; telophase transforms each of the two daughter nuclei produced into a new interphase-metabolic state. Figs. 1, a-l represent these stages of mitosis as seen in the root tip meristem of the onion plant Allium cepa; Figs. 2, a-d are similar stages of the first cleavage mitosis in developing eggs of the horse round worm Ascaris megalocephala.
Prophase represents the stage of division in which all the mitotic components are mobilized prior to their organization into a characteristic metaphase configuration. One of the most important of events that takes place during this phase is the transformation of the chromatin ‘network’ of the interphase-metabolic nucleus into morphologically distinct units, the chromosomes, the structure of which was discussed in Part I. This transformation is brought about mainly by the imposition of a series of coils upon the chromosome thread (see Fig. 6, Part I), and as prophase progresses the chromosomes, at first long and thin, become much shorter and thicker as the coils gradually increase in size and compactness and become reduced in number. How this spirilization phenomenon is brought about is not very well understood; it has been suggested as being brought about by changes in a chromosome's DNA molecules. Obviously, however, it is very important to mitosis for it enables the chromosomes to move and separate with little risk of entanglement and subsequent disruption of movement.
As well, two other noticeable changes take place during prophase, the breakdown of the nuclear membrane and the loss of the nucleolus. The nuclear membrane is broken down into small
See Sampson, Tuatara Vol. 11/3, 1963.
The reason for the disappearance of the nucleolus is not understood. One concept suggests that an exchange of material occurs between the nucleolus and the chromosomes, or perhaps an exchange involving the spindle apparatus, but no conclusive evidence is available concerning this. It is known for certain, however, that the nucleolus is important to the preparatory events of mitotic prophase, for point irradiation of the nucleolus prior to prophase inhibits mitosis, yet once the nucleus has entered prophase no such inhibition can be brought about.
If present, as in many animal cells, the duplicated centriole, lying just outside the nuclear membrane before prophase, becomes visibly active during this phase, its duplicates separating at the start of prophase and gradually migrating round the nuclear membrane to take up positions opposite each other, so fixing the poles of the cell (Fig. 2a). Though we know little of these movements barring the probability of the activity of phenomena similar to those found at anaphase, and involving spindle elements, one must mention that these centrioles are important guiding elements to which anaphase chromosomes migrate. They appear to have an important bearing on all the organizations that follow prophase. In plant cells and many animal cells where centrioles are not distinguishable the poles, no doubt, are also fixed during prophase.
At even the early stages of prophase the chromatids of each chromosome are often distinguishable. The chromatids are the units that will separate to opposite poles at anaphase (Fig. 1f) and become the chromosomes of the daughter nuclei produced. They have been formed by exact duplication during preparations for division, preparations which are considered in more detail below.
After the completion of prophase transformations the chromosomes become arranged along the equator mid-way between the two poles to form the so called ‘metaphase plate’. This orientation phase, involving marked movements of the chromosomes, is referred to as prometaphase and its result as metaphase.
The start of prometaphase coincides with the completion of the breakdown of the nuclear membrane towards the end of prophase. During prometaphase the chromosomes move, the centromeres leading these movements, dragging as it were the chromosome arms behind. At its completion the two chromatid centromeres of each chromosome lie one above and one below the equator, one directed to one pole, the other to the opposite pole; they have become co-oriented.
Not only are the chromosomes oriented during prometaphase; the spindle apparatus is as well. Spindle material, manufactured during preparations for division and often seen in living and fixed cells as a clear zone surrounding the outside of the prophase nuclear membrane, is organized into an array of ‘fibres’ extending from pole to pole and pole to centromeres (See Fig. 12, Part I). Indeed these two discriptively distinct orientations are, as we shall discuss later, intimately associated with each other.
Metaphase is the climax of mitosis for here the chromosomes are poised ready for their actual feat of division. At this stage we can see most of the structures that interact to accomplish this division; the two chromatids lying alongside each other; the two centromeres of each chromosome in a co-oriented position; the poles, marked in many cases by centrioles; the chromosome spindle fibres connecting the centromeres to their appropriate poles, and the continuous fibres from pole to pole. Metaphase passes into anaphase as this machinery is set into activity to bring about an orderly and exact mitosis.
Anyone who has followed a living cell through mitosis under the microscope or watched a cine-micrograph of mitosis could not have failed to have been impressed at the unique movements that the chromosomes, literally huge macromolecules, show during anaphase. Even examining a series of static preparations as shown here, one is suitably impressed. Indeed these movements have been the cause of not just a few cytologists pondering in almost complete bewilderment; and today much has still to be learned about anaphase mechanics. This aspect of anaphase is discussed later.
At metaphase the sister chromatid centromeres of each chromosome are co-oriented in the equator so that they are engaged by spindle fibres from opposite poles. During anaphase the spindle fibres and centromeres, and undoubtedly other cell
f), the chromosome arms appearing to be dragged behind (Fig. 1h). Each chromosome moves quite independently of the others though as initiation generally affects all chromosomes together, anaphase takes the form of two groups of chromosomes separating to opposite
The events that take place during telophase are essentially the reverse of those that are found in prophase. The nucleolus is gradually reformed through the organization of material at a locus on the nucleolus organizing chromosome; a nuclear membrane is reassembled, here one round each daughter nucleus; and the chromosomes gradually lose their coils and a fine ‘network’ of chromatin is formed. The nuclei are transformed into a typical interphase-metabolic state.
The division of the cytoplasm whereby complete daughter cells are produced is most commonly geared to occur in the late anaphase-telophase of mitosis and between the two separated groups of chromosomes so that each cell produced from a complete cell division is in a uninucleate condition. The process of cytokinesis typically associated with cell division is achieved in one of two rather distinct ways, by cell plate formation or by furrowing, the former characteristic of plant cells, the latter mostly of animal cells. In animal cells the cell membrane, a somewhat elastic structure, becomes pinched inwards all around along the position of the cell equator (Fig. 2d). This furrow so produced gradually extends inwards and eventually cleaves the parent cell into two.
Plant cells are surrounded by a comparatively rigid cell wall and so cytokinesis by furrowing is apparently impossible. Instead, cell wall material is laid down at the centre of the equator, and as cytokinesis proceeds, increasing amounts of such material forms a so called cell plate that grows outwards towards the parent cell walls until it cuts the cytoplasm in two (Fig. 1k). Differentiation along each side of the cell plate forms a new partition between the two daughter cells.
The plane of division as indicated corresponds exactly to the equatorial plane as fixed by the position of the poles in the previous prophase. This relationship becomes clear if at metaphase the poles and spindle apparatus is not centrally placed in the cell.
An unequal placement of the mitotic apparatus takes place under normal conditions during some patterns of tissue development following the movement of the nucleus to one end or side of the cell prior to division, and displacement of the spindle has been induced artificially with a microneedle. As a result, unequal cells are produced.
It might be asked further whether or not the spindle apparatus itself is important in bringing about cytokinesis. Present evidence through experiments on the removal or disruption of the spindle elements at various stages of mitosis suggests that the relationship between spindle and cytokinesis is indirect rather than direct; the fixing of the poles during prophase determines on one hand the spindle and its equator, and on the other hand the plane of cytokinesis. The correspondence between the spindle equator and plane of cytokinesis alone, though, suggests a possible functioning of spindle elements in cytokinesis. Some hypotheses in this respect have been suggested.
Mitosis accomplishes more than simply making two cells out of one. It is a very exact process whereby the daughter cells formed have the same number and complement of chromosomes in their nuclei. By the very early stages of division each chromosome has duplicated itself into two identical halves (chromatids), and prometaphase orientation and anaphase separation ensure that these halves pass to opposite poles. This reproduction/co-orientation/separation occurs in every chromosome of the parent nucleus and so the daughter nuclei produced after division have come to possess identical chromosome complements and, therefore, identical gene complements. They are genetically identical.
The importance of division in the cytoplasm is also more profound than a glance might merely suggest; we understand it as being very important to cell differentiation. Prior to embarking on cell division it is understood at present that a cell may become polarised within its cytoplasm, i.e. localized parts of the cytoplasm may take on different forms (e.g. in structure, enzyme content, chemical composition, metabolic activity). After nuclear division cytokinesis may accentuate this polarity by segregating these differences into different cells, so that, in contrast to their nuclei, daughter cells come to have quite distinct cytoplasms. This is believed to be the basis of how two genetically identical cells can diverge in their paths of differentiation to give rise to distinct structural and functional tissues.
Mitosis is nature's plan for growth and differentiation: it also forms the basis for the accomplishment of the aims of meiosis.
The distinctiveness of the process of meiosis can be appreciated from a study of the products of this division as well as from a study of the cytological features of the process itself. Two principal differences single out meiotic products from those produced through somatic mitosis. Firstly, they possess the haploid rather than the diploid complement of chromosomes; and secondly, depending on a number of factors we will consider below, each nuclear product is unique in its gene make-up. These two differences reflect on a number of very distinct cytological features that can be recognized from a study of the process; and two quite unique phenomena distinguish meiosis from somatic mitosis — synapsis and crossing-over. Meiosis hinges on these two features.
The meiotic products are four in number and meiosis consists of two nuclear divisions (meiosis I and meiosis II) accompanied by only one division of the chromosomes. These two divisions then bring about a reduction in the chromosome number and at the same time, as we shall see, they reshuffle the genes that homologous chromosomes bear and thus stamp individuality on the genetic make-up of their products. Figs. 3, a-r represent successive stages of a meiotic division as found in pollen mother cells of the onion weed Allium triquetrum.
As with somatic mitosis it is convenient to discuss the process of meiosis under the headings of five phases, prophase through to telophase. Prophase of meiosis I is termed prophase I to distinguish it from the prophase of meiosis II, or prophase II; likewise for the other phases of the two meiotic divisions.
The key to meiosis is found in prophase I, indeed, in the two phenomena referred to earlier as synapsis and crossing over. These two events involve prophase I in a complex series of phenomena and the phase is consequently divided into five subphases, leptotene, zygotene, pachytene, diplotene and diakinesis. As prometaphase follows prophase of somatic mitosis so prometaphase I follows diakinesis of prophase I in meiosis.
During prophase I the nuclear chromatin becomes transformed into chromosomes as in somatic mitosis, the nucleolus likewise gradually disappears, and the nuclear membrane breaks down. This transformation, basically one of coiling, is much more marked than that of mitosis (probably due largely to the prolongation of the prophase stages) and the chromosomes at diakinesis are thus much more compact than their corresponding somatic chromosomes (compare Figs. 3d and 4b). Chromosome contraction begins at leptotene, and continues through to diakinesis. Zygotene is the stage of division during which synapsis occurs (Fig. 5). Recall from Part I of this article that a diploid organism carries two homologous sets of chromosomes in its body cells, one derived from its male parent, the other from its female parent; the two chromosomes of each pair are homologous in morphology and basic gene make-up. Synapsis is the pairing of these homologous chromosomes, not at random but arm with arm, centromere with centromere, chromomere with chromomere and probably (though it cannot be certain) gene locus with gene locus. The intimacy of synapsis is clearly demonstrated in the band to band pairing of the salivary gland chromosomes of Drosophila discussed in the first part of this article.
At pachytene synapsis is complete so that each pachytene thread is in fact made up of two chromosomes closely paired throughout their lengths so as to appear as one. A feature of these pachytene chromosomes is their logitudinal ‘beaded’ nature (Fig. 3b) which in some cases (e.g. in maize chromosomes) may show quite distinct patterns and permit identification of particular chromosomes in the complement.
It is not until the following phase, diplotene, when the homologous chromosomes begin to fall apart or desynapse that we can consider further what has taken place prior to or at pachytene. The homologous chromosomes desynapse at diplotene along their lengths except at certain regions termed chiasmata (chiasma, singular). These chiasmata (Fig. 6) are considered to be responsible for maintaining the association of homologous chromosomes until they separate at anaphase I; and it will be seen also that the orientation of the chromosome pairs prior to anaphase is similarly dependent on the chiasmata. Chiasmata govern a regular meiosis. But what are these chiasmata?
Towards the end of diplotene, and in some cases earlier, chromosomes can be seen to be double, each composed of two chromatids. These chromatids have been formed earlier as a result of chromosome duplication. And at this stage also, more can be seen of the exact nature of the chiasmata; each represents a locus where two chromatids, one from each of the two previously synapsed homologous chromosomes, exchange pairing partners or ‘cross-over’ (Fig. 6). How this crossing over is brought about
Diplotene chromosomes take on a characteristic ‘shaggy’ appearance (Figs. 3c and 6) which is not clearly understood, though it is probably related to a particular metabolic state within the diplotene nucleus and is presumably indicative of intense activity between chromosomes and cytoplasm, activity which is almost certainly concerned with past or future events in the division cycle.
The chiasmata hold together pairs of homologous chromosomes, or bivalents as they are usually called. At diakinesis, when the chromosomes reach their maximum contraction, the bivalents can usually be readily counted; their number corresponds to the haploid number of chromosomes of a particular species for bivalents consist of an associated pair of chromosomes. There are nine bivalents in Allium triquetrum (Fig. 3d).
By diakinesis the loss of the nucleolus and breakdown of the nuclear membrane are complete and the bivalents, usually distributed at random, pass into their phase of orientation.
As in somatic mitosis the chromosomes, as pairs or bivalents here, move during prometaphase I into co-oriented positions along the equator, midway between the two poles. This orientation, however, does not involve chromatid centromeres as in mitosis. Sister chromatid centromeres in a bivalent act as one and we can say that bivalent orientation involves centromeres of homologous chromosomes. As a result of this, metaphase I takes on a rather distinct appearance when compared with that of mitosis (c.f. Figs. 3e and 1d), though basically they can be considered the same. In mitosis chromatid centromeres are oriented to opposite poles, while the chromatids remain together associated at regions adjacent to the centromeres and along the chromosome arms. In prophase I of meiosis the bivalent centromeres are oriented to opposite poles, and the chromosomes remain associated by their shared chiasmata. The variable position of the chiasma nearest the pair of centromeres in a bivalent determines the distance these centromeres become separated at metaphase I and thus the appearance of the oriented bivalent as a whole (Figs. 3e and f).
At metaphase I the bivalents are poised ready for anaphase separation for at this stage the spindle apparatus has likewise become organized. A careful thought will indicate what, compared with mitosis, will segregate at anaphase (see Fig. 7). This is important.
As with metaphase I., anaphase I of meiosis takes on distinctive characters, though essentially the process is the same as in mitosis. During anaphase I the co-oriented centromeres of each bivalent move apart to opposite poles, at the same time forcing the chiasmata along towards the ends of the bivalents as cross-over portions of chromatids peels off from their sister portions (Fig. 7). Each centromere carries with it two chromatids and by mid-anaphase the chiasmata have been lost and the chromosomes freed (Fig. 3g). By the end of anaphase I, when movements cease, the homologous chromosomes have become widely separated, and Telophase I phenomena (Fig. 3i), essentially the same as those of telophase in mitosis, then transform the two chromosome groups into two interphase nuclei (Fig. 3j). Note that each transforming group of chromosomes consists, not of a diploid number of single chromosomes (cf. mitosis) but a haploid number of double (chromatid) chromosomes.
The nature of the meiotic interphase that follows telophase I varies in different species between two extremes. At one extreme the interphase chromatin becomes very diffuse as is found after a mitotic division, and nucleoli and nuclear membranes fully reform. In the other extreme telophase is not completed but
Allium triquetrum approaches the first extreme (Fig. 3j) though the spoke-like arrangement of the chromosome arms, imposed through the convergence of the centromeres on the poles during the previous anaphase, is carried over into the early second division stages (Fig. 3k).
The meiotic interphase must be recognized as being quite distinct from that which follows a mitotic division or precedes a meiotic one. At this phase there is no chromosome duplication for the chromatids that are to separate during meiosis II have already been formed. They were formed at the very early phases of meiosis. Here then we see clearly the essence of meiosis as a reduction division — two divisions with only one duplication.
Perhaps, since duplication has already occurred and duplication appears to require the chromatin to be in an interphase state (see later), the prolonged interphase, as found in Allium triquetrum, is a vestige and of no use. However, it must be remembered that in some species additional metabolic activity, dependent also on an interphase state of the chromatin, might have to be undertaken before meiosis II can begin; and these species would then possess a meiotic interphase of some completeness and duration.
Also during telophase I and interphase cytokinesis usually takes place to form two complete daughter cells from the original parental cell. Following this each of these two daughter cells will ‘go it alone’ and pass (though often synchronized) into the second stage of meiosis in order to complete the reduction in chromosome number that was initiated in the first division.
During meiosis II each sister cell produced from meiosis I divides into two following the separation of the two chromatids of each chromosome into alternate nuclei. The characteristic tetrad of products thus results from a complete meiotic division.
Meiosis II can be divided into prophase, metaphase, anaphase and telophase II and these stages are very similar to those found in somatic mitosis. Some important differences should be noted, however. Firstly, the chromatids of prophase and metaphase II are those already formed by the early stages of prophase I, and secondly, they are widely separated from each other except at their centromere regions. Thirdly, individuals of a pair of chromatids are not genetically identical. This inequality has been brought about through crossing over and will be discussed again later.
Mechanically, meiosis II is essentially the same as somatic mitosis. The chromosomes contract during prophase II (Fig. 3k); they become oriented along the cell equator during prometaphase
l and m), and the spindle is organized; the chromatids of each chromosome then pass to opposite poles, headed by the centromeres and mediated through spindle activities during anaphase II (Fig. 3, m-p) and telophase II transforms the groups of chromosomes into interphase-metabolic nuclei (Fig. 3q). Cytokinesis is again geared to telophase and through it the formation of four meiotic products is completed (Fig. 3r).
Meiosis II completes the reduction of the chromosome number that was initiated during meiosis I: without either division reduction is not achieved. The reason why we cannot consider that the chromosome number has been halved at the end of meiosis I is because the chromosomes at this stage are double for, disregarding crossing over, meiosis I has separated the products of synapsis, not the products of duplication. The products of duplication separate at anaphase II. Meiosis I and meiosis II are complementary divisions, and for this reason the latter must never be considered as simply a somatic mitosis following on from a division regarded as the reductional sequence.
The essential characteristics of meiosis will be seen from Fig. 7. both in respect of its reduction from a diploid to haploid complement of chromosomes (cf. Figs 4a and b), and its reshuffling of chromosome segments.
One of the most important of the preparations undertaken for mitosis is clearly the duplication of the chromosomes, for without this mitosis could not possibly proceed in any regular manner. As a result of chromosome reproduction the two chromatid units involved in anaphase separation are formed; and each anaphase chromosome, if ultimately passing through a following cell division, will duplicate itself to form another two chromatids for that division.
Chromosome reproduction can be studied with the use of radioactive materials that are incorporated into either the protein or DNA components of chromosome structure; the radioactivity permits their identification, localization, distribution and time of incorporation. Many such studies in recent years have provided very valuable information regarding the duplication phase of mitosis. One of the most interesting of the results has shown that chromosome reproduction as measured by DNA and protein synthesis takes place during the interphase-metabolic state of the nucleus, and the chromatids of mitosis are thus formed well in advance of the initiation of division. Recently it has been suggested that the interphase metabolic nucleus can be divided
1, S, and G2, and in root tip meristems of the broad bean Vicia jaba e.g., these three phases are of about equal eight hour periods. S is the phase of chromosome duplication; G1 is a ‘gap’ between the end of a previous cell division and the start of chromosome duplication; and G2 is a second ‘gap’ between the finish of chromosome duplication and the time when the nucleus enters prophase of mitosis. As might be expected there is no uniformity in different species in the time of the beginning or ending of the S period in relation to G1 and G2, but it is clear that the major part of chromosome duplication always takes place during interphase.
Does the same situation hold in meiosis? A few cytological observations suggesting the doubleness of leptotene chromosomes have been followed up in recent years with the finding that DNA synthesis for chromosome duplication does occur largely in the premeiotic interphase nucleus, and chromosomes have already duplicated by the very early stages of prophase I. Crossing over in meiosis involves the chromatids of each chromosome so it is clear that this phenomenon occurs after, or at least at, the time of chromosome duplication. It seems too that synapsis at zygotene occurs when each chromosome consists of two chromatids. These two aspects related to chromosome reproduction will be discussed again later.
What can be said of the G1 and G2 periods in regard to preparations for mitosis? The relative metabolic inertness of the chromosomes during mitosis suggests that during the interphase-metabolic nucleus, parallel paths of metabolism operate to build up all the necessary components involved in mitosis prior to prophase initiation. One such pathway in chromosome reproduction has already been mentioned. Another concerns the spindle apparatus. Experiments indicate clearly that molecules which are built up to form the metaphase spindle are manufactured as precursor molecules during interphase and are held in readiness for their prometaphase orientation as distinct structures. We have indicated this already for spindle material becomes apparent as a clear zone surrounding the prophase nucleus prior to the breakdown of the nuclear membrane.
Though only fragments of information are available, inhibition and other experiments strongly point to the concept that mitosis
A final word on preparation for division should be given concerning the centrioles. When present the centriole of each nucleus duplicates very early in the cycle of cell division. Indeed they begin to duplicate at the closing telophase stages of a mitotic division, and thus represent the earliest cytological indication of a forthcoming mitosis.
All these and undoubtedly other preparations for cell division set the stage for the initiation of mitosis. This initiation is considered in a little detail below.
Two periods typify cell division, a period of preparation and a period of mitotic activity. The distinctiveness of these two periods can be appreciated from a number of facts. There are for instance, a number of known cases in which chromosomes have entered mitosis without becoming duplicated: the mitotic events that follow are irregular, but apparently only because the singleness of the chromosomes inhibits co-orientation and anaphase separation. Then there are a number of ‘spindle poisons’ such
How does a nucleus precipitate into mitosis after its preparatory period? And what initiates subsequent periods of preparation? Unfortunately, particularly from the point of view of uncontrolled cell division in malignancy, the answer is not clear. A relationship must clearly exist between growth (cell size) and division; hormones will stimulate many dormant and mature tissues to become meristematic; but it seems, however, that no mitotic ‘trigger’ alone sets cell division into motion, but rather a number of different metabolic pathways lead a cell to mitosis. In other words, successive interactions between the nuclear genes and the cytoplasm create intracellular environments that lead to activities related to cell division. Thus one event leads to another and so on to set the environment that will eventually lead to mitotic activity.
The other problem to mention is the transition from somatic mitosis to meiosis. Here, however, the basic questions remain largely unanswered too. The unique events of meiotic prophase I presumably reflect on characteristic physiological conditions in the cytoplasm that bring about a meiotic rather than a mitotic division, though numerous attempts to induce meiosis or inhibit it have not been helpful in solving the problem.
Prophase I of meiosis is often described as being precocious compared with somatic mitosis in that it is early in its initiation and its spindle formation in relation to its chromosome production. This precocity hypothesis of Darlington's is still much debated among cytologists. It is based on the assumptions that leptotene chromosomes are not duplicated and that homologous chromosomes pair in order to satisfy a ‘need’ for prophase chromosomes to be associated in pairs. In mitosis the association of sister chromatids satisfies this need. In meiosis synapsis brings satisfaction. Present evidence from chromosome duplication does not entirely fit this hypothesis, though in the absence of challenging suggestions and with certain modifications it still holds wide acceptance. A little more will be said concerning this hypothesis under the section on synapsis.
The process of pairing of homologous chromosomes is the most marked cytological phenomenon that distinguishes meiosis from
It is clear that under normal circumstances synapsis occurs specifically between chromosomes that are homologous, and that the phenomenon is quantitatively limited to two's. In polyploid
pairs of segments. It was this aspect of chromosome behaviour in polyploid cells that led Darlington to consider that prophase chromosomes must be in a paired state to be ‘stable’. This state is considered to be satisfied in mitosis by chromosome duplication to chromatids, and in meiosis by synapsis of chromosomes. On the completion of chromosome duplication during synapsis the paired state is presumed to be now satisfied through the association of sister chromatids, and homologous chromosomes therefore desynapse; as we have noted they do at diplotene.
From the brief consideration above on meiosis in polyploids, it will be apparent that the units of synapsis are not homologous chromosomes, but rather homologous segments of chromosomes. Indeed, observations in organisms with sufficiently large and clear pachytene chromosomes show that chromomere pairs with chromomere very specifically, and in Drosophila salivary gland chromosomes, a specific chromatic band pairs with its homologous band. What the lower size limit is to the unit of synapsis is of course debateable; it is often considered that chromosomes possess a pairing face composed of many molecular sized synaptic units.
Synapsis is initiated some time after the start of meiotic prophase and the chromosome thread is already in a partly coiled condition when it sets in. This fact complicates any model of synapsing chromosomes one tries to imagine and must be considered in any elaborate thoughts on the nature of the forces of synapsis. At initiation the homologous chromosomes are first brought into apposition at one or a few places, and pairing then continues from these ‘contact’ points in a zipper-like fashion. Contact points are usually at regions of the centromere and chromosome ends. In the majority of organisms there appears to be no time limit for zygotene and hence synapsis is complete, though cases of localized unpaired segments are known. As would be expected, in abnormal haploid cells undergoing meiosis unpaired chromosomes regularly appear during the division as only one of a particular type of chromosome is present. The very rare occurrence of interlocking bivalents at diplotene and diakinesis presents somewhat of a problem when analysing the process of synapsis.
The problem of the nature of the forces of synapsis will best be appreciated from a consideration of whether long range forces are operational over considerable distances, or only short range forces after chance association at contact points.
It is difficult to ascertain the spatial distribution of chromosomes preparing to undergo synapsis so that little is known of the distances that might separate members of a pair of homologous chromosomes; regular synapsis in a cell undergoing meiosis immediately following fertilization Some simple animals and plants have haploid somatic cells, produce gametes by mitosis, and meiosis immediately follows fertilization.
On the other hand it has been thought that movements of prophase chromosomes (which have been observed in a number of living cells) may be sufficient to bring about chance contact
Finally, from a physical point of view there has been some thought on what kind of forces (e.g. Van der Waal's) might be necessary to operate synapsis over long and short distances, but these must be considered largely speculative at present. The difficulty here is that generalized attraction between chromosomes is not sufficient to account for the specificity of synapsis; a great many different forces must be operative, each for and characteristic of one particular pairing locus. Whatever forces or models of synapsis are hypothesized they must as well take into account many other characteristics of the synaptic phenomenon, some of which are mentioned above.
Crossing-over, both from a cytological and a genetical point of view, holds a unique and most important place in the process of meiosis; through it the two aims of meiosis that have already been stressed are realized. As with the discussion on synapsis above it is advisable here to clearly point out a number of basic features of crossing-over before giving a few indications of the mechanics involved in the process.
From a theoretical point of view alone it will be clear that crossing-over between homologous chromosomes must produce products (chromatids) that are exactly reciprocal to each other; otherwise the integrity and homologous nature of a pair of chromosomes could not possibly be maintained from generation to generation, for just one unequal crossing-over would produce one chromatid duplicated for certain segments while the other would be deficient for these segments. Genetic studies have shown quite definitely that exact reciprocal products are indeed normally formed. This feature of crossing-over suggests a close relationship between it and the high specificity already noted in synapsis; what this relationship is will be considered below.
The second point to consider is that the chromatid, not the chromosome, is the unit of crossing-over (Fig. 6). At any one point along the chromosome pair only two of the chromatids are involved in recombination and each of the four chromatids that ultimately segregate in the two divisions of meiosis conies to have its own unique chromosome make-up (Fig. 7). But although at any one point only two chromatids cross-over, all four may become involved if more than one cross-over is formed. If we label the four chromatids A, A' (sisters) and a, a' (sisters) then four cross-overs might involve chromatids A and a' at one point, A and a at another, then A' and a', and finally A' and a. How many cross-overs are possible and do arise between a chromosome pair, then?
The cross-shaped configuration between two non-sister chromatids at diplotene and later stages is known as a chiasma (Figs. 6 and 7) and we have assumed that it represents a cytological manifestation of a genetically determinable crossing-over, i.e. a chiasma is the result of a cross-over. A great amount of evidence points to the correctness of this assumption. The most convincing support comes from recent work with meiotic cells in which one of a pair of homologous chromosomes has an abnormal form (e.g. a terminal piece lost; or a piece that has become inverted). If a single cross-over occurs in the chromosome arm containing this abnormality then certain distinctive chromosome configurations can be expected to occur at anaphase I (Fig. 9); and the observed 1: 1 correspondence between the percentage of these configurations and the percentage of bivalents with single chiasmata at metaphase I, taken from a large number of cells, is what can be expected if a chiasma represents a cross-over. There is a lot of additional and equally strong evidence from diverse studies in support of this idea and few cytologists today have any doubt as to its essential correctness. A cross configuration as in Fig. 6 would result if during diplotene desynapsis pairs of sister chromatids fell apart on one side of the X locus, and pairs of non-sister chromatids on the other side. This of course would not represent a genetic cross-over and would not produce anaphase configurations as in Fig. 9. There are some cytological indications that such or other types of ‘pseudo-chiasmata’ may arise in certain cases.
A priori, the number of chiasmata in a bivalent should be an indication of the number of cross-overs that have arisen. However, in a large number of organisms a gradual reduction in chiasma number occurs between diplotene and metaphase I. This reduction is brought about by a process known as terminalization, caused through the movement of a chiasma to a more distal position, so causing its neighbours to fuse or to be lost. The process of terminalization is essentially the same as that occurring in anaphase I as illustrated in Fig. 7. though in the former ‘repelling’ forces of desynapsing chromosomes are thought to be the main cause, whereas polar centromere movements bring it about at anaphase.
Another feature concerning crossing-over and chiasmata is the phenomenon known as interference — the suppression by one cross-over of the occurrence of others within a short adjacent segment. There is much cytological evidence from chiasma studies and genetical evidence from crossing-over data for the expression of such a phenomenon. It must clearly influence the number of chiasmata that can arise within a bivalent. A peculiar feature is that suppression does not appear to cross the centromere, i.e. a cross-over in one arm appears to have no suppressing effect on another in the other arm.
From the above comments it will be evident that a number of factors affect crossing-over and chiasma frequency. Large chromosomes often have three, four or more chiasmata per bivalent, while other equally large ones may have only one or two. Smaller chromosomes generally have fewer chiasmata. Except in a few very specialized cases, one chiasma must arise in each bivalent, for upon this chiasma hinges the continued association of the two chromosomes and their subsequent orientation and segregation.
Studying bivalents at diplotene (Fig. 6) one gets the strong impression that crossing-over and chiasma formation is brought about by a process of breakage and reunion so that reciprocal portions of sister chromatids become united (Fig. 7). Chromosome breakage and reunion are known to occur spontaneously (and can be induced) outside meiosis, but whether or not such a process occurs in crossing-over and chiasma formation has not been entirely proven. Darlington has suggested that at chromatid formation during pachytene, tensions in the coiled chromosomes cause localized breakages and reunions, but there is little positive evidence for such an interpretation. Another hypothesis suggests that ‘errors’ in chromosome duplication at pachytene lead to crossing-over, i.e. chromatids are formed of material reproduced from parts of both, rather than from one of the two synapsed chromosomes. This hypothesis requires chromosomes duplication to occur at pachytene and thus does not entirely fit available data (see page 61.).
The exact reciprocal nature of crossings-over and the high specificity of synapsis suggests that the former occurs at the completion of the latter, or in other words, crossing-over occurs at pachytene. This is visualized in the two hypotheses mentioned above. But though crossing-over involves the chromatids of a chromosome it may occur during chromosome reproduction prior to pachytene synapsis. and not necessarily after duplication. This clearly presents other problems as some sort of association of homologous chromosomes is a pre-requisite for crossing-over, but recent hypotheses suggest that contact occurs between homologous chromosomes during the interphase of meiosis and at a time when the chromosomes are duplicating. ‘Errors’ in duplication then give rise to crossing-over. These hypotheses fit the available evidence more satisfactorily, but much uncertainty still remains. For a new concept see Moens (1964).
While little is positively known about the mechanics of crossing-over, a great deal has been learned of its effect. Crossing-over undoubtedly results in an exchange of segments of homologous chromosomes as illustrated in Fig. 7 and the result is clear; with only one chiasma in one bivalent the four products of meiosis come to differ in their chromosome make-up, and thus in their genetic make-up. For a fuller appreciation of the reason for this the reader is referred to any textbook on first principles of genetics.e.g. GENETICS, by R. P. Levine Modern Biology Series, 1962.Homo sapiens, each with many genes, each with a minimum of one chiasma at meiosis; then witness the variation between individuals of the progeny of such a species!
A most important factor governing a regular division of the nucleus in meiosis and mitosis is the co-orientation of the chromosome or bivalent centromeres to form the so called metaphase plate. In each case, one of the two associated pairs of centromeres is directed to one pole, the other to the opposite pole, and from this position anaphase will proceed in the necessary orderly fashion. This co-orientation is very clear at meiotic metaphase I (Fig. 3e)
The very important studies in recent years of mitosis and meiosis in living plant and animal cells have provided a great deal of information regarding prometaphase movements. They show conclusively that the centromere is the organ of movement of the chromosome. And it is evident from irradiation and chemical inhibition studies that these movements are basically the same as those found at anaphase, being brought about through interactions between centromere and spindle. A very clear illustration of this comes from the use of drugs (e.g. colchicine) that inhibit spindle activities. They inhibit anaphase separation; they also inhibit metaphase orientation, and the cells are blocked at the end of prophase. The nature of the interactions between centromeres and spindle that are necessary for orientation will be considered in more detail in the next section. In essence they bring about an orientation of spindle substances from a diffuse state round the prophase nucleus to a highly organized series of ‘fibres’ extending from centromeres to pole; and they bring the chromosomes into a position to form a regular metaphase plate. The interactions appear to start with a contraction stage where the scattered chromosomes suddenly form a tighter mass before the more specific movements begin. This start seems to coincide with the loss of the nuclear membrane, a probable indication of the initial incorporation of spindle substances into the nucleus.
What is most interesting concerning the mechanics of prometaphase is that a chromosome or bivalent may not move directly onto the equator in a co-oriented position. It may do so, but it may first move to one or the other pole, then perhaps to the other pole before becoming stabilized along the equator.
These movements suggest that each centromere (of bivalent or chromosome) is capable at one time of an orientation and movement to one pole, and that from this basic property the two types of movement of an associated pair of centromeres indicated above
With a chromosome or bivalent oriented and at one pole, a phenomenon of re-orientation appears to operate to achieve its subsequent co-orientation. If one of the two centromeres re-orientates to the opposite pole the bivalent or chromosome will move to the equator in a co-oriented position. Re-orientation of both centromeres would cause the bivalent or chromosome to move to the opposite pole and further re-orientation would have to be undertaken before achieving co-orientation.
Whether or not these ideas are in fact the basis of prometaphase mechanics has yet to be ascertained, and a lot of aspects remain to be understood.
One aspect that should be apparent is that for co-oriented centromeres to remain in the equator and for polar chromosomes or bivalents to be brought into the equator following re-orientation, two features are necessary. Firstly, the chromosomes of a bivalent, and chromatids of a mitotic chromosome must be linked together. This linkage is provided by the chiasmata in the former, and by some little understood substance or structure in the latter; co-orientation depends on pairs of chromosomes or chromatids so linked. Secondly, the magnitude of the ‘force’ acting between a centromere and pole must very directly with the distance separating the two; the greater the distance, the greater the force. Metaphase centromeres must be in an equilibrial position. There is a lot of evidence available for this assumption.
There are other aspects of prometaphase mechanics that are not well understood. Why, for instance, do chromosomes not clump into the centre of the cell at metaphase but remain regularly spaced out? Repulsion forces are perhaps important. And why do some chromosomes show preferences for particular positions along the equator? These and other questions remain largely unanswered, and the reader is referred to Schrader's book ‘Mitosis’ for a comprehensive analysis of these and related problems.
The movement of the chromosomes from the equator to the poles during anaphase is probably one of the most intriguing yet most puzzling of biological movements. Since mitosis was first described its theme has been constantly discussed and many theories have been put forward in explanation. Space, however, will not permit mention of most of these and it must be admitted that this important phenomenon still eludes complete understanding.
Firstly, the importance to chromosome movements of the centromere and its associated spindle fibres is today clearly recognized. A chromosome without a centromere or whose centromere has been deactivated by point irradition fails to move, and similar maltreatments of the spindle by X-rays or poisons likewise inhibit anaphase. Secondly, the chromosome spindle fibres shorten as anaphase progresses and it is clear that centromeres and spindle interact to accomplish chromosome movements; and since each chromosome moves independently of the others, it is individual centromeres and their associated spindle elements that interact for this purpose.
The concept that a chromosome is passively dragged in movement by the shortening of fibres attached to its centromere and based at a pole can no longer be considered as a possible mechanism of chromosome movement in the light of present day evidence. Birefringence studies have indicated that a wave of activity precedes the centromere as it moves to the pole, and other evidence also points to the conclusion that the centromere is a very active organ in bringing about chromosome movements.
What can be said of the chromosome apart from its centromere?
Studies in living material have shown that in mitosis the whole chromosome is active during the initiation of anaphase. The two sister chromatids, that up to anaphase are closely associated along their lengths, appear to relax their attraction for each other before the centromeres actually begin to peel the chromosome arms away from each other to opposite poles. Since all the chromosomes in a cell are simultaneously affected in this way it seems very likely that this is an indication of a change in the chromosome environment that triggers anaphase and permits further centromere/spindle activity for polar movements. Similar activities can be thought of as being present at the initiation of anaphase in meiosis as well, though here not affecting the chromosome regions adjacent to the centromeres until anaphase II. However, it should be remembered that the fact that the chromosome segments between centromere and chiasmata are often stretched during anaphase I (Fig. 3f) indicates that the chiasmata afford considerable resistance to chromosome separation, a resistance that would not be expected if all attraction between chromatids were lost at initiation. Chromosomes in anaphase of mitosis show no such stretching. Yet by mid-anaphase I of meiosis the chromatids of each chromosome are usually widely separated from each other except at their centromeres (Fig. 3g).
In meiosis II, anaphase initiation is centred round regions of the centromeres where the chromatids previously maintained association.
Two systems of movement are at present considered to operate after the initiation of anaphase. The first has already been indicated; that observable cytologically as a shortening of the spindle fibres and a movement of the chromosomes towards the poles. The second is an increase in the distance between the two poles which, while not moving the chromosomes nearer to the poles, increases the distance between the two separating groups of chromosomes and thus contributes significantly to anaphase: this phenomenon is readily observable cytologically if centrioles are present, but otherwise as an increase in the lengths of the pole to pole fibres of the spindle. The relative importance of these two systems varies with the organism; the latter appears characteristic more of animal rather than plant cells, though in both the former is considered to be the most important.
During anaphase a physical and/or chemical change appears cytologically to take place in the interzonal region between the two separating chromosome groups. Whether this is a third phenomenon associated with anaphase movements is not clear. It may be related to a ‘pushing’ action acting between the chromosome groups; or it may be more related to cytokinesis rather than to anaphase.
To close this section a few comments should be made on the nature of the important forces of anaphase; those associated with centromere/spindle activities. It is no longer acceptable today to consider the spindle fibres as series of protein threads that become folded during anaphase and thus draw the chromosomes nearer the poles. Rather, the spindle fibres are considered at present to represent regions of general spindle molecules that are in a highly oriented state (thus appearing as fibres); and that perhaps a change in this oriented state, brought about by the centromere, results in chromosome movements. Before more elaborate explanations can be given, however, a great deal must yet be learned of the physical and chemical changes that precede and accompany anaphase, a field that is only just being pioneered. Elusive though these explanations are, there is no call for dispair for little more is known of the perhaps equally or more interesting action of muscle tissue or other forms of biological movements. Some further indication of the problems concerned and the type of research they stimulate will be had from reference to Schrader's book on ‘Mitosis’ and the more recent articles by Mazia in ‘The Cell’ and those from the Second Conference on Cell Division.
Considerable data have become available in recent years on the duration of mitosis, of its various phases, and of the associated intermitotic time, and while generalizations tend to be misleading they give some indication of upper and lower limits. Rarely does
The prophase of meiosis is of much greater duration than the prophase of a corresponding mitosis. This fact may be related to the suggested precocious nature of prophase I already discussed.
As far as division in its completeness is concerned, a cell spends a large proportion of its time in preparations between successive mitoses. This is particularly so in meristem tissues where the cells maintain a near constant volume through successive division cycles (Fig. 1l). The length of the intermitotic time is clearly of importance to cell growth: in the first number of cleavages of a developing egg cell, mitosis follows mitosis very rapidly, intermitotic times are short, and successive daughter cells become increasingly smaller in size.
The time course of the various stages of mitosis and meiosis can be well appreciated from the numerous movie films on cell divisions, films that also vividly dramatize the swift and decisive movements of the chromosomes.
It has been impossible in this article to cover all aspects and problems associated with cell division and to mention all evidence, for and against, concerning those features I have discussed. But it is hoped that the article has indicated something of the level of present-day understanding of this important biological process, and will stimulate thought for further enquiry. For this latter purpose a brief list of appropriate books is given below.