EVOLUTION OF CHROMOSOME NUMBERS
AND CHROMOSOME FORM

GEORGE C. W ILLIAMS : Adaptation and Natural Selection

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The Lepidoptera have a greater range In chromosome number than any other group of animals (from n = 7 to n = ca. 220). But they show a strongly marked mode at 29 - 31 so that the variance is much lower than in the decapod Crustacea. A subsidiary mode at 23-24 is due to the family Lycaenidae ('Blue' butterflies), the only family of Lepidoptera with a clearly marked mode of its own, different from that of the group as a whole. The distribution of chromosome numbers in the Lepidoptera is clearly skewed and asymmetrical about the mode, there being far more species with numbers below twenty-nine than there are ones with numbers above thirty- one. In other words fusions seem to have been considerably more frequent (or more successful in an evolutionary sense) than dissociations, in this group of insects. Individual genera of Lepidoptera include some in which all or almost all the species have the same chromosome number. Thus about fifteen species of Papilio have n = 30, only a few having other numbers such as n = 27 or 31 (Maeki and Remington 1960a), almost all members of the tribe Nymphalini have n = 31 and all members of the Limenitini have n = 30 (Maeki and Remington 196lb).

On the other hand we have many genera and tribes of Lepidoptera in which extreme variations in chromosome number occur. Thus the three species of the remarkable Giant Skippers (Megathymidae) that have been investigated have haploid numbers of 21, 27 and 50 (Maeki and Remington 1960b). In the genus Erebia, the primitive chromosome number was probably about 28 or 29, as in other genera of the family Satyridae (Maeki and Remington 196la). But some species have very much lower numbers such as n = 7 in E. aethiopellus and n = 8 in E. calcarius ; and some have considerably higher numbers such as n = 40 in E. ottomana and n = 51 in E. iranica and E. dromulus (Federley 1938 ; Lorkovic 1941 ; de Lesse 1955, 1959b). In this genus, apparently, both fusions and dissociations can establish themselves in evolution. In the lycaenid genus Lysandra, however, (Lorkovic 1941 : de Lesse 1953, 1954, 1959a, 1969, 1970) dissociations seem to have been spectacularly successful, but there is no evidence that fusions have occurred at all. This genus includes a few cytologically primitive species with n = 24 such as L. syriaca (the usual number in the family Lycaenidae) and a series of species with the haploid numbers 45, 82, 84, 88, 90. 124, 131-150, 190- 191 (in L. nivescens from Spain) and 217-223 in L. atlantica from Morocco (the animal species with the highest chromosome number known). The very closely related lycaenid genus Agrodiaetus, however, includes species such as A. posthumus (n = 10) and A. araratensis (N = 13) in which fusions have established themselves and others like A. phyllis (n = 79-82) in which many dissoociations have occurred (de Lesse 1957. 1959c).

It is not only in these Old World Lycaenidae that spectacular evolutionary changes In chromosome number have taken place. Such New World members of the Lycaenidae as Hemiargus hanno (n = 14), Calephelis virginiensis (n = 45) and Lycaena heteronea (n = 68) show wide deviations from the modal number, and so do such Japanese species as Taraka hamada (n = 1 5) and Ussuriana stlygiana (n = 47) (de Lesse 1967; Maeki and Remington 196la). In the family Pieridae, the Euchloini have a modal number of 31 and the Pierini one of 25- 26. However, a few divergent species occur in this family also. Thus Pieris brassicae has n = 15 and an African Leptosia n = 12 (Maeki and Remington 1960b). In the Nymphalidae, most species of Vanessa, including Japanese individuals of V. indica, have n = 31 (Maeki 1961), but Indian material of this species shows n = 15 according to Y. Gupta (1964) ; probably the two forms should be regarded as distinct species. Two species of Actinote (subfamily Acraeinae) from Bolivia show the widely different chromosome numbers n = 14 and n = ca. 150 (de Lesse 1967).

In a number of lepidopteran species with high chromosome numbers numerical variations have been recorded. Most of the work has been done on first metaphases, so that what has been counted are the visible bodies (no doubt mostly bivalents but in some instances possibly univalents or multivalents) rather than single chromosomes. Unfortunately, there seems to be no means of distinguishing between univalents, bivalents and multivalents in lepidopteran spermatogenesis - they all look like small spheres or isodiametric bodies in which no structure is observable. Some of the numerical variation in these species is no doubt due to the inherent difficulties of the work, i.e. it is due to less than perfect technique. Thus, when de Lesse reports that Lysandra argester from various localities in Spain and Savoie show a variation from n = 147 to n = 15 1 we may legitimately suppose that the apparent variation is due to imperfections in technique, although this conclusion does not necessarily follow and it may be that some real variation occurs. When, however, he adds that four individuals of the same species from high elevations in the Sierra Nevada of southern Spain show n = 131 -134 it is clear that he has discovered a geographic race with a lower chromosome number. Different populations of Agrodiaetus dolus from Italy, southern France and Spain show n = 108, 122 and 124 (de Lesse 1966a).

Spectacular evolutionary changes in chromosome number have occurred in moths as well as butterflies. Thus Suomalainen (1963, 1965) has Investigated forty species of the large geometrid genus Cidaria. Thirteen of them had n = 31, and 32 had numbers between n = 28 and n = 32 ; but species with 19, 17 and 13 chromosomes also occurred. The chromosomes are obviously larger in the species with lower chromosome numbers and photometric measurements show that the total amount of DNA is approximately the same in spite of the great differences in chromosome number. This shows clearly that we are not concerned with polyploidy. More extensive and accurate determinations of the DNA values of species that have undergone large scale increases or decreases of chromosome number in the course of phylogeny are badly needed ; it is to be expected that species whose chromosome numbers have increased (e.g. L. nivescens and L. atlantica) will show higher DNA values and ones with diminished chromosome numbers (e.g. Agrodiaetus posthumus) lower than average DNA values, if we are correct in assuming that these evolutionary changes in chromosome number have been due to dissociations and fusions. On a somewhat different footing are those instances where genuine variations in chromosome number have been recorded within demes or within individuals. Intrademic variation without intra-individual variation is likely to be entirely genuine, and in some instances both phenomena may really coexist. Just what the explanation is in species like Leptidea sinapis, where Lorkovic (1941) has recorded n = 26-41 , is uncertain. Supernumerary chromosomes might be involved, but it seems more probable that the species is polymorphic for a number of chromosomal fusions or dissociations, since L. morsei shows n = 54, L. amurensis n = 61 and L. duponcheli n = 104 (Lorkovic 1941 ; Maeki 1958a, b). It seems useless to speculate about such cases until they have been critically reinvestigated, with determinations of the total amount of DNA present.

In considering the processes which have been involved in the evolution of unusually high or low chromosome numbers in the Lepidoptera, we may first of all rule out polyploidy, since there is no real suggestion of polyploid series in such genera as Erebia, Lysandra, Agrodiaetus. Furthermore, as pointed out earlier (White 1946c) many of the species with very high numbers have one bivalent which is much bigger than the others, or several large bivalents which differ visibly in size - i.e. karyotypes that exclude any possibility of straightforward polyploidy. And, although DNA values have not been determined, several authors (e.g. Y. Gupta 1964) have noted that where two closely related species or greographic races of Lepidoptera differ greatly in chromosome number, the chromosomes of the one with the lower number are much larger, so that the overall volume of the metaphase chromosomes is similar -which is what we should expect if fusions or dissociations have occurred. It is, of course, possible to maintain that polyploidy has occurred but has then been complicated by further karyotypic changes that have obscured the evidence for it. But there is no justification for such unnecessarily complicated hypotheses. On the contrary, it now seems clear that lepidopteran species with extremely high or low chromosome numbers represent the end products of evolutionary processes, each step of which was an increase or decrease of the chromosome number by one element. The extreme case is Lysandra atlantica, which has presumably accumulated 193 to 199 dissociations since the lineage to which it belongs diverged from the main stock of the 24-chromosome lycaenid butterflies. There is still some doubt as to whether localized centromeres are present in lepidopteran chromosomes and it may be that a holocentric condition is usual. But in any case each dissociation would have required a donor chromosome (to provide telomeres, even if centromeres were not needed), and the final result would be a species carrying much duplicated genetic material, perhaps mainly heterochromatic.

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