on speciation in ice age mammals, with special reference to cervids and caprids

0 1 1 speciation in Ice Age mammals, with special reference to cervids and caprids

VALERIUS GEIST The University of Calgary, Faculty ofEnvironmentn1 Desigrt , Cnlgan, Altci., Canada T2N IN4

Received May 28, 1986

GEIST, V. 1987. On speciation in Ice Age mammals, with special reference to cervids and caprids. Can. J. Zool. 65: 1067- 1084. Five types of species can be identified in large mammals. The evolution of three types. Ice Age giants, island dwarfs, and

hybrids, can be explained, but not that of tropical food specialists and continental paedomorphs. Ice Age giants, which arose while colonizing latitudes (altitudes) with increasingly seasonal climates and productivity pulses, are characterized by ornate social organs, large bodies, and ecological plasticity. Colonizing landscapes with decreasing seasonality appears to conserve (or re-evolve) primitiveness, producing paedomorphs. Island dwarfs appear to be shaped by efficiency selection in the absence of predators. The explanation of mammalian Ice Age evolution hinges on the sensitivity of mammals to environmental factors, in particular nutrition. Extremes in food abundance generate extremes in phenotypes and selection regimes. Abundance is linked to colonization and selection for new social and ecological adaptations; scarcity is typical of settled areas and maintenance regimes. These select for efficiency in the procurement, processing, and use of food. Rapid speciation is predicted during colonization, followed by agradual, continuous fine tuning of the ecology of the new form. Neither the punctuated nor the gradualistic model of speciation adequately explains evolution in large mammals. Early predictions of the "dispersal hypothesis" of mammalian evolution have now been tested for caprids. Results from cytogenetic, electrophorectic, and immunodiffusion studies support the dispersal hypotheses.

GEIST, V . 1987. On speciation in Ice Age mammals, with special reference to cervids and caprids. Can. J. Zool. 65 : 1067- 1084. Les grands mammifkres peuvent 2tre classifies selon cinq types d'especes. L'evolution de trois de ces types, les gCants de

l'kpoque glaciaire, les nains insulaires et les hybrides, peut s'expliquer assez bien, mais celle des spkcialistes alimentaires tropicaux et celle des pedomorphes continentaux s'expliquent mal. Les geants de I'ipoque glaciaire, apparus par colonisation des latitudes (altitudes) a climats et a productivite de plus en plus saisonniers, ont des organes sociaux ornementes, un corps de grande taille et font preuve de plasticit6 Ccologique. La colonisation de regions a saisonnalitk decroissante semble assurer la conservation (OU une nouvelle evolution) de propriktes primitives, produisant ainsi les pedomorphes. Les nains insulaires semblent silection- nCs pour leur efficacitk en l'absence de predateurs. L'explication de l'kvolution des mammifkres au cours de l'epoque glaciaire s'appuie sur la dependance des mammiferes vis-a-vis des facteurs Ccologiques, en particulier de la nutrition. Une situation extreme quant a l'abondance de la nourriture genkre des phinotypes et des regimes de silection extremes. L'abondance est liee a la colonisation et a une sklection favorisant des adaptations sociales et Ccologiques nouvelles ; la rarete est typique des regions ktablies et des regimes de maintien. Ceux-ci font une selection en fonction de I'efficacite de la recherche et de l'utilisation de la nourriture. Durant la colonisation, il faut s'attendre a une speciation rapide suivie d'un ajustement graduel, continu et subtil de l'kcologie de la nouvelle forme. Ni le modele ponctuk, ni le modele gradualiste de la spkciation n'expliquent adequatement 1'6volution des grands mammifkres. Les predictions antkrieures decoulant de << I'hypothese de la dispersion H en kvolution des mammifkres ont it6 iprouvees chez les Capridks. Les resultats obtenus li l'analyse cytogknetique, a l'klectrophorkse et a l'ktude de l'immunodiffusion appuient les hypotheses de dispersion.

[Traduit par la revue]

Truth, Sir, is a cow, which will yield such people no more milk, and so they are gone to milk the bull.

Samuel Johnson, 2 1 July 1773

Introduction How do large mammals speciate? I found neither the conventional gradualistic nor the con-

troversial punctuated model of evolution of great help in answering that question. The gradualistic model, in its selec- tionist form, fails to address the fact that phenotypes, not genotypes, are the raw material of natural selection (Wadding- ton 1957). It consequently ignores epigenetics (Lovtrup 1977), fails to distinguish between adjustment and adaptation, and encourages contrived "just so" stories and a simplistic view of genetics, development, and evolution.

The punctuated model fails to show a mechanism that could adequately account for rapid speciation; it is vague on what happens between an old form disappearing and a new form arising (Eldredge and Gould 1972; Gould and Eldredge 1977; Vrba 1980; Stanley 198 1; Eldredge 1985). This transition is proposed to take place on the periphery of a species range, but just that is predicted by the classical gradualistic model. If, for instance, two related species meet and form barriers to reproduction (Mayr 1966), a "speciation event" would take place. It should be revealed in the fossil record as a sudden divergence of

characters in the two species, and the disappearance of the parent forms. Related species can only meet at their peripheries. The punctuationists have thus inherited Goldschmidt's (1940) "hopeful monster" problem, of not being able to explain in adequate detail how a "new design" arises out of an old one. Not many transitions between fossil faunas have been found, and those that have been found have said little about the process of speciation (Williamson 198 1). Ironically, while the two views are contested by paleontologists and the controversy continues (Gingerich 1984), both schools imply that the record provided by fossils cannot help in gaining sufficient insight into the process by which species come to be (microevolution). It thus appears that the fossil record cannot be of much help in elucidat- ing how species form, in part because of its coarseness, but also because of other difficulties such as those identified by Churcher (1984).

In a study of wild sheep I formed an explanation of their evolution that led to the work reviewed here. At first I called that explanation "glaciation theory" (Geist 197 la), but soon re- labeled it "dispersal theory" (Geist 197 1 b), as it held promise of broad application. This theory described in detail a mechanism that rapidly creates "novelty" in the external appearance of large mammals by changing their social organs. The dispersal hypothesis, as it should have been named, has been repeatedly upgraded (Geist 1978a, 1978b, 1983, 1986b). While it initially resembled what later came to be known as the punctuated

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1068 CAN. J . ZOOL. VOL. 65. 1987

equilibrium model, it soon diverged to show when and how gradualistic evolution should occur. It also differed by being based on neontology, not paleontology, although it made predictions that could be tested by paleontologists (Geist 197 1 a: pp. 343-34.6). Paleontology was vital, however, in showing the direction of evolution. I found that one could not speak of the process of speciation, since more than one type of species could be identified, and therefore more than one process could be generating species.

The dispersal hypothesis centered on two phenomena, the epigenetic plasticity of large mammals and social behaviour. The former is an old but neglected field of knowledge, dispersed among a number of disciplines. The hypothesis is highly specific to large mammals and the idiosyncracies of their biology. I cannot claim universality, but I do claim that while it relies heavily on ungulates, the hypothesis is applicable to hominids (Geist 1 9 7 8 ~ ) .

The dispersal hypothesis revolves about a duality of phenotypes that arise at the extreme ends of material resource availability. Luxury generates the dispersal, shortages the maintenance or efficiency phenotypes. The former condition leads rapidly to hypermorphic species via social selection during dispersal into increasingly seasonal environments; chronic shortages fine tune maintenance phenotypes progressively to be more efficient in procuring and processing resources. This leads to gradual changes in morphology as individuals become better at doing "more with less." Dispersal into environments with decreasing seasonality appears to lead in a symmetric fashion to paedomorphism and the retention (or re-evolution) of primitiveness.

As I hope to show, the dispersal hypothesis has power of explanation in dealing with Ice Age mammals and Pleistocene evolution. It fails, however, to account for the type of mammals found in the tropics. For instance, it is silent on how the same body plan diversifies into a multitude of ecological specialist species that live sympatrically. It explains only how diferent body plans evolve as large mammals radiate from the tropics.

In the development of this hypothesis, I have had to cross disciplinary boundaries and juxtapose concepts and language from different fields. That detracts from ease of reading, as do attention to a certain amount of unavoidable detail and deviation into needed explanations. I found that sketches help to bring across points, and have included some relevant ones in this review.

To understand the dispersal hypothesis, one must turn to what it attempts to explain, namely the regional variation in social organs.

Clinal variation in large mammals Many species of large mammals exhibit altitudinal or latitu-

dinal clines. The mule deer (Odocoileus hemionus) of western North America shows a cline (Fig. 1) that stretches from sea level (most primitive form) to the high altitudes of the Rocky Mountains. The races change in body size, antler size and complexity, configuration of the rump patch and tail, and size of the metatarsal glands (Cowan 1936). The smallest race, that most closely resembling the white-tailed deer, is the Sitka deer ( 0 . h. sitkensis), which lives along the ocean shores in a cold, wet climate with high winter snows, and a landscape densely covered with coniferous rain forest. Moving southward, we encounter dry, warm coastal ranges in California where we find the Columbian black-tailed deer ( 0 . h. colurnbianus); north of Los Angeles the cline swings inland to the western slopes of the

Sierra Nevada, occupied by the California mule deer ( 0 . h. californicus). The Inyo deer ( 0 . h. inyoensis) occupies the eastern slopes of the Sierra Nevada, and beyond that the large Rocky Mountain mule deer ( 0 . h. hemionus) radiates north to the Yukon, east to Manitoba, and south to Sonora in Mexico. It occupies, in its large distribution, a broad range of continental and desert climates, but shows no noticeable clinal variation therein.

The Old World deer offer vivid examples of latitudinal and altitudinal diversification. Note the sika (Cewus nippon), red deer (Cervus elaphus), and wapiti (C. e. sibiricus-nelsoni) (Fig. 2) in the oversimplified cline. These deer, which are distantly related to New 'Norld deer, show similar changes to those found among mule deer: body size, antler complexity, and rump patch and tail configurations change together, as does the social behaviour (Geist 1982) and voice of the rutting stags (Tembrock 1965; Nikolski and Wallschlager 1983; Nikolski 1984); body shape changes as a function of the mode of locomotion. Sika deer are saltatorial runners and red deer are saltatorial-cursorial, while the wapiti are the most cursorial of living Old World deer (Gambaryan 1974). Ecologically these deer vary by choos- ing increasingly more open habitats, and feeding increasingly on grasses. The size of tooth rows thus increases (Szunyhoghy 1963; Hutton 1972). The cline in Fig. 2 lacks the radiation from the hangul-type stags (Fig. 2B) to the European type stage, of which I have illustrated only the east European form (Fig. 2F). From east to west, the antlers of the European red deer change by branching in the terminal fork. The number of terminal tines per antler changes from 2 to 4 to 8, and the total number of tines in fully mature heads is ideally 10, 14, and 22. While all European red deer have the same rump patch, the west elaphines grow, in males only, a large, dark neck mane; the east elaphines retain a light coloured, short-haired neck.

Between the animals illustrated in Figs. 2C and 2D, another cline branches off, namely that of the West Chinese and Tibetan red deer. These converge toward wapiti in antler form, in both sexes having a neck mane, in the stags retaining their antlers a very long time and beginning the rut immediately after shedding velvet, and in a reduction in sexual dimorphism in body size (Engelmann 1938; Allen 1940).

One can find a convergence not only between two branches of red deer toward the wapiti body form and mode of life; one can also find it between unrelated branches of Old World deer. The white-lipped deer (Przewalskium albirostris) is a rusine deer (Flerov 1952) quite different from deer of the genus Cervus (Groves and Grubb 1987) and yet, as an occupant of the open Tibetan plateau it has evolved remarkably toward the wapiti in external appearance (Fig. 3) and antler mass.

Similar geographic variation occurs in other ruminants, but also among other large-mammal lineages (Geist 197 1 a , 197 1 b, 1978a, 1983). One can recognize a pattern: in warm climates there are species of a primitive body plan, but ecologically diversified and highly specialized. In the temperate zones there follow species of more advanced body plans, which are replaced at higher latitudes by species of still more advanced body plans. Thus within-latitude evolutionary radiations create ecological variations on the same body plan; between latitudes, evolution alters body plans. Within-latitude evolution differentiates ecological specializations; between-latitude evolution shapes social organs (hornlike organs, rump patches, tails, external glands, hair coat patterns, body colouration, vocal and visual signals). The Old World deer illustrate this well.

In tropical and subtropical latitudes, Old World deer are

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FIG. 1. Clinal variation in body size and social organs (antlers, rump patch and tail configurations, metatarsal glands) in the mule deer (Odocoileus hemionus). (A) Sitka deer ( 0 . h. sitkensis); (B) Columbia black-tailed deer ( 0 . h. ~~olumhianus); (C) California mule deer ( 0 . h. californicus); (D) lnyo deer ( 0 . h. inyoensis); (E) Rocky Mountain mule deer ( 0 . h. hemionus). For explanation. see text. (To scale, after Cowan 1936.)

FIG. 2. Clinal variation in sika and red deer. (A) Sika deer (Cervus nippon); (B) hangul (Cervus elaphus afinis). (C) Buchara stag (C. e. bactrianus); (D) Izubr stag (C. e. xanthopygo.~); (E) wapiti (C. e. sibiricus-nelsoni; (F) east European red deer (C. e . maral). (After Engelmann 1938; Allen 1940; Heptner et al. 196 1 ; Geist 197 1 h.)

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CAN. J. ZOOL. VOL. 65 , 1987

FIG. 3. Convergence in altitudinal (A) and latitudinal (B) evolution in distantly related Old World deer. (A) Tibetan white-lipped deer (Przewalskium albirostris) and (B) wapiti from Siberia and North America. (After Geist 1983 .)

structured on the old, primitive two- and three-pronged antler plans (Fig. 4). They have long tails, no rump patches, and very little in the way of hair coat pattern or colour diversity. Rusa and Axis have large subhypsodont molars, much larger than those of northern species, reflecting ecological specialization. In temperate zones one finds deer with an evolved, four-pronged antler plan. Beyond that are deer with more complex antler and body plans, so that the terminal species in extreme climates tend to be recent, ornate giants of their respective lineages. Contrast the primitive sika and the advanced wapiti (Fig. 5) or the extant but primitive fallow deer (Duma duma) and the extinct but advanced terminal species of that lineage from periglacial environments, the giant deer (Megaceros giganteus) (Fig. 6). The wapiti and the giant deer are of fairly recent origin (Kurten 1968; Geist 197 1 b; Azzaroli 1979).

The geographic progression in deer just described is roughly paralleled by the temporal progression from the mid-Tertiary to the late Pleistocene (Fig. 7). That is, two- and three-pronged deer antlers precede four- to six-pronged antler plans in time, while large, complexly antlered deer are of Pleistocene age. We can thus be fairly certain of what is primitive and advanced in Old World deer, and that deer evolved latitudinally from south to north. However, matters are more complex than meets the eye.

Note in the sheep cline (Fig. 8) that the Armenian mouflon (B) fits into the cline between Ammotrugus (A) and Ovis arnrnon cycloceros (C) as if it were a primitive form. However, karyotype analysis shows that with 2n = 54, it is derived from the primitive 2n = 58 chromosome condition (Nadler et al. 1974). Mouflonlike sheep also appeared rather late in Pleis- tocene times in Europe (Kurten 1968), an indication that they are rather recent forms. It appears that we have here an example

FIG. 4. Tropical Old World deer of the second and third pronged antler stage of evolution. (A) Muntiacus: (B) Axis porcinus; (C) Axis axis; (D) Rucervus duvauceli; (E) Rusa unicolor. (After Geist 1983.)

FIG. 5. The extant subarctic giant and the temperate zone, primitive dwarf of the cewine lineage of Old World deer. (A) Wapiti; ( B ) sika.

of a paedomorphic dwarf, that is, a species exhibiting a sharp reversal to ancestral characteristics. (By contrast, the clinal changes discussed are examples of asynchronous hypermorph- ism in Gould's ( 1977) terms.)

It thus appears that species are formed (i) via ecological specialization within a latitude and landscape, (ii) via social evolution between latitudes and (or) altitudes, and (iii) into paedomorphic dwarfs (probably when dispersal is reversed, occurring from north to south). In addition we note (iv) dwarfed large mammals on islands (Azzaroli 1982) and ( v ) the possibility of related populations forming new types via hybridization. The latter shall not concern us further, but we may note in passing that while ecological differentiation may occur sympatrically (in a broad geographic sense), social differentiation latitudinally occurs allopatrically. Thus, forms generated by the latter process are more likely to hybridize upon meeting than forms shaped by speciation in contact with similar forms. Thus sika deer and red deer hybridize not only where they are brought

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FIG. 6. The periglacial giant and the temperate zone, primitive dwarf of the megacerine lineage of Old World deer. (A) Giant deer Megaceros giganteus; (B) fallow deer Dama dama. The giant deer is reconstructed from cave paintings of the upper Paleolithic according to Meroc and Mazet (1953) and R. D. Guthrie (personal communication).

together by the hand of man (Kiddie 1962; Harrington 1973; Lowe and Gardiner 1975), but also naturally, where they occur sympatrically (Heptner et al. 196 1 ); indeed, karyotype studies now show that continental sika deer may well have strong red deer admixture (Bartos et al. 198 1 ; Bartos and Zirovnicky 198 1, 1982). The high rate of splitting of ecological "specialists" is not for discussion here; see the excellent paper by Vrba (1980) on this topic.

Comparing the geographic dispersion of several lineages, one notes a parallel: species of comparable evolutionary status are found together (Fig. 9). In caprids, Ovis and Capra tend to pair off at comparable stages of evolutionary development, primitive with primitive, advanced with advanced (Geist 1985~) . An evolutionary dispersal may also be radial, as in the ibex (Nievergelt 1981) but also in American bighorn sheep (Geist 19856). One can also compare periglacial species, all of which tend to be "grotesque giants" of their respective lineages, Homo sapiens included (Geist 1978a, 1983). Conversely, no matter what lineage, all tropical giants tend to be based on old, primitive plans, but are specialized ecologically. The foregoing indicates that latitudinal-altitudinal speciation can take place in several co-colonizing species simultaneously.

The geographic variation encountered is not necessarily genetic. Many old and new studies elucidate the nature of variation in mammalian morphology; much of the work has been done by animal scientists, beginning with J. Hammond's (1 960) work, but there have also been studies by continental scientists work- ing primarily on red deer (Ingebrigtsen 1923; Vogt 1936, 1948; Vogt and Schmidt 195 1; Beninde 1937; Gottschlich 1965; Szunyhoghy 1963). It is likely that the fivefold spread in body mass between European red deer populations is purely environmental! A review suggests that genes communicate with the environment through the phenotype, adjusting it adaptively (Geist 1978a: pp. 1 16- 144). Similar views were expressed by Balon (1979, 1984) and James (1983). Body size and body shape change greatly in allometric fashion with the net income in material resources of the individual during ontogeny.

FIG. 7. The progression of Old World deer in time from the mid- Tertiary to the Pleistocene. Antler plans progress from the two- to the six-tined plan. Each antler plan appears in three versions: simple, with supernumerary tines, and palmate (west European red deer often carry a four-pronged, supernumerary tined antler, not illustrated). (A) Primi- tive, tusked, nonantlered Oligocene deer; (B) Eustylocerus, mid- Miocene; (C) Dicrocerus, early Miocene; (D) Stephanocemu.~, mid- Miocene; (E) Axis, early Pliocene; (F) Rucervus, time of origin un- known; (G) Cervavitus, late Miocene; (H) Cervus (sika), Villafran- chian; (J) Anuglochis, Villafranchian; (K) Cervus elaphus acoronatus, the first red deer of Europe, early Pleistocene; (L) Cervus elaphus mural, late Pleistocene red deer; (M) Dama dama, mid-Pleistocene; (N) C. e. sibiricus-nelsoni, wapiti; Recent and late Pleistocene; ( 0 ) Eucladoceros, late Villafranchian; (P) Megaceros giganteus, late Pleistocene. (After Thenius and Hofer 1960; Godina et al. 1962; KurtCn 1968; Geist 197 1 b.)

Genomes can give rise to extremes in phenotype development; with resource shortages arise an environmental paedomorph (maintenance phenotype), with resource abundance a luxurious hypermorph (dispersal phenotype). These extremes differ di- ametrically in morphology, social behaviour, reproduction output, and demographic factors, so that maintenance phenotypes emphasize efficiency in utilizing material resources as well as competing for those material resources. Dispersal phenotypes, freed from resource shortages, maximize reproduction, social competition, exploration, and dispersal (Fig. 10). To develop

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CAN. J . ZOOL. VOL. 65, 1987

FIG. 8. Clinal variation in African and Asiatic ovines. (A) Barbary sheep (Ammotrclgus), North Africa; (B) Armenian mouflon (Ovis orientalis gemelini); (C) Afghan urial ( 0 . ammon cycloceros); (D) Arkal(0. o. arkal); (E) Severtzou's urial ( 0 . o. severtzovi); (F) Marco Polo's sheep ( 0 . ammon poli); (G) Tienshan argali ( 0 . a . karelini); (H) Altai argali ( 0 . a . ammon). (After Geist 197 la , Fig. 43.)

full-fledged dispersal phenotypes requires several generations in The signal for dispersal phenotype development was pre- overcoming "maternal effect," a discovery we owe to Vogt's dicted to be the protein content in the gestating female's diet (1948; Vogt and Schmidt 1951) work on deer, and substantiated (Geist 1978a: pp. 139- 144). This was found to be the case by since (Denenberg and Rosenberg 1967; Chandra 1975; Beach et Chauvez and Martinez ( 1979). One can also expect considerable al. 1982). One can thus expect great changes in body size and osteological variation due to differences in the type of muscular size-related shape changes in large mammals. forces exerted on bones (Du Brut and Laskin 1961). The ex-

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TROPICS

TEMPERATE ARCTIC

FIG. 9. Cervids vary geographically in the same direction, primitive with primitive forms, advanced with advanced froms. From left to right: European, Manchurian, and east-Siberian forms. Bottom: Cer- vus elaphus mural, C . e . xanthopygos, C . e . sibiricus. Middle: Alces alces alces, A. a . cameloides, A. a . gigaslpfitzenmayeri. Top: Cap- reolus capreolus, C . pygargus bedfordi, C . p. pygargus. (After Geist 1986b.)

PHENOTYPES

MAINTENANCE

FIG. 10. Phenotype extremes in ontogenetic development as a function of resource availability. Maintenance phenotypes arise under conditions of low resource availability; dispersal phenotypes arise under conditions of resource abundance. This is a schematic illustration incorporating the "centripetal theory of growth" of animal science (Wilson 1952, 1958; Hammond 1960), and the "paedomorphic-hypermorphic" theory of European investigators beginning with Ingebrigt- sen ( 1923). Note differences in body proportions.

perimental work on variation in large mammal morphology has given us tools to segregate environmental and genetic variation.

Body size varies in large mammals latitudinally and altitudi- nally with the duration of the "production pulse" (Fig. 1 1 ) (Guthrie 1984; Geist 1986b) and not with its height as originally suggested by Margalef (1963). In essence, the productivity pulse provides a holiday from resource shortages; it is zero in constant climates with constant productivity, it reaches its maximum duration somewhere in the temperate zones, and it de-

FIG. 1 I. (A) The annual productivity pulse in relation to food availability and requirements for maintenance and growth. For the time period T I -T2, an individual would experience superabundance of food and a release from food resource competition. (B) Conceptual model of productivity pulses in the tropics, temperate zones, and arctic. The period of superabundance varies in curvilinear fashion latitudinally, being shortest in tropical and arctic climates. (After Margalef 1963; Geist 1978a, 19866; Guthrie 1984.)

clines in length towards the Arctic. Body mass is expected, therefore, to increase latitudinally, but then reverse (Fig. 12) so that small-bodied forms occur at high and at low latitudes. Since antler and horn size tend to be large and positive allometric functions of body size, large regional differences in antler size and morphology may be expected for environmental reasons. One can judge whether antler shape differs genetically between two populations only by examining the largest bodied males, and even then it is safest if the males to be compared are experimentally raised under identical conditions. One such clas- siial study (vogt 1948) on the nutrition and growth of red deer shows that west elaphines (represented by stages of Silesian red deer (western Poland origins)) and east elaphines (represented by Hungarian red deer) do indeed differ in antler structure, as I described earlier.

Although systematic experiments on the relationship between temporal patterning of nutrition and the shape of antlers are missing, incidental observations suggest that such a relationship exists. Instructive are Vogt's (1948) findings of how food shortages early in World War I1 affected the antlers of his ex- perimental animals. lllness and injury can cause considerable change in antler growth (Goss 1983). During ontogenetic development in males the basic antler structure of young males is repeated in regressing old ones. Put simply, small antlers are paedomorphic irrespective of the age and body size of their bearer. All this indicates that the social organ, the antler, can vary greatly with many environmental factors that need to be carefully considered before drawing taxonomic, let alone evolutionary, inferences.

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0-

Q Rangifer

Odocoileus virginionus -- 4 lslond Odocoileus virginionus --

0d2 0!3 0)4 015 0)6 017 018 019 1'0

RELATIVE BODY MASS

FIG. 12. The duration of access to superabundant food (TI-T2 in Fig. 11) is related to body size as illustrated in three genera of New World deer. Body size varies curvilinearly with latitude, not linearly as stated by Bergmann's rule (Geist 1986b, 1986~) .

Let me illustrate with a crass example: antler length of extant fallow deer (Mehlitz and Siefke 1974), the mid-Pleistocene Riano fallow deer (Leonardi and Petronio 1976), and the giant deer (Megaceros giganteus, Gould 1974) falls along the same line predicted by condylobasal (skull) length:

[ 1 ] beam length (mm) = 0.0039 (condylobasal length, mm)2. ' l 4

The palm width of Megaceros is predicted by the palm width of Riano fallow deer antlers (Leonardi and Petronio 1976)

[2] palm width (mm) = 0.001 39 (beam length, mm)'.706

Also, the antler plans of old Riano fallow deer stags are identical with those of young Megaceros stags (as illustrated by Owen 1846: Figs. 184- 186); both differ from old Megaceros stags in that the latter have one additional radial branching so that the number of tines doubles (excluding tine 4; see Fig. 7). Extant fallow deer differ from the Riano deer and Megaceros by having relatively wider palms as if achieved through additional radial branching confined to the palm. For extant fallow deer,

[3] palm width (mm) = 1.94 x 1 o - ~ (beam length, mm)2.096

This indicates that Megaceros antlers had the length, width, and number of antler tines one would expect from a fallow deer of the same size. As long as Magaceros bulls were able to supply the prodigious daily requirements in protein and minerals to grow 35-45 kg of antler mass, they would grow antlers of said pattern. Consequently, no case can be made that Megaceros antlers evolved beyond the Riano fallow deer stage. Their size and shape appear to be explained purely by the body size increase of Megaceros. Since antlers tend to spread with size (i.e., in wapiti, Hutton 1972), it is not even certain that the great spread of Megaceros antlers is an "evolved" or simply an ontogenetic feature. Unfortunately, no data exist for Riano fallow deer on the relation of beam length to antler spread to test this hypothesis. The above assumes that Megaceros was a giant fallow deer, a conclusion raised early and repeatedly, and hotJy contested (Gould 1974). Current information indicates fairly

FIG. 13. Antler mass as a function of metabolic size ((wt. in kg)' ") plotted against absolute body mass in mature New World deer males. Forest deer cluster along the line linking roe, white-tailed deer, and European type moose. Deer living in open landscapes, such as mule deer and caribou, but also the American type moose of Beringian origin in Pleistocene times, all have much larger antler masses (Geist 1986b, 1986~) .

- V)

k 5 0 - - k I 2 g 200 - > L3 0 m 150 - 0 -Y u

\ 0 -- 100 - cn cn a r 5 50 - -J k z a

0

conclusively that Megaceros was a fallow deer (A. Lister, personal communication).

Since hornlike organs are such a conspicuous part of the evolutionary change in latitudinal-altitudinal lineages of ruminants, it is necessary to dwell briefly on their function, before any attempt is made to explain their evolution. The first class of hornlike organs consists of short, sharp stilettos, the very kind of weapon associated with the defence of material resources on a territory (Geist 1978a, 1978b). Complex antlers fall into another category of hornlike organs, namely those borne by gregarious open-country forms. They are weapons whose pri- mary function is no longer to maximize (painful) surface damage, but to catch and hold the head of an atacker, and to permit wrestling (Geist 1966, 1978b, 1978a: pp. 74-80). Also, in both Old World and New World deer, forest forms carry significantly less antler mass at comparable body weights than do forms from the savannah (Fig. 13). One notes another, similar difference in antler mass between tropical and temperate or cold zone deer of comparable size and habitat preference.

Savannah deer carry 1.5-2.0 times the antler mass of rela- tives living in forests. This is the same order of magnitude as the increase in neonatal investment by the females; neonatal invest-

A 0 American Moose + European Moose ' ' V Manchurian Moose White tailed Deer ' P a m p a s Deer

m I I I I 1 I I

ment increases from forest to savannah and steppe (but declines in climatically harsh landscapes; Fig. 14). This leads to the prediction that antler mass and neonatal investment are positive- ly related (Fig. 151, as are antler mass and the percent milk solids produced by the female in mid-lactation (Fig. 16). In open landscapes with high predator densities, it pays to have young that minimize the duration of the dangerous postnatal period, when they are small, slow, and of low stamina. Here the young must be born large and grow rapidly to survivable size as speedy endurance runners. Therefore, the most cursorial deer ought to have the largest young at birth, the largest antler mass, and the richest milk. This fits the most cursorial living deer, Runglfer. The most cursorial deer ever was Meguceros gigunteum (Geist 19860). The following suggests that increasing relative antler and horn mass in latitudinal-altitudinal evolution may be linked

0 100 200 300 400 500 600 700

WEIGHT (kg)

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Single

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COVER SAVANNAH STEPPE DESERT TUNDRA ALPINE

FIG. 14. Relative birth weight in ungulates increases from forest to steppe, but declines in desert, tundra, and alpine habitat. The trend holds for single as well as multiple births. Sample sizes are given in parentheses, bars extend one standard deviation each side of the means, and vertical lines give the ranges (Geist 1986~) . Neonatal mass calcula- tions after Geist (198 1). 1 kcal = 4.1868 kJ.

FIG. 15. Relative neonatal mass correlated with antler mass. 1 . 0docoileu.s virginianus; 2, 0 . hemionus; 3, Capreolus c-apreo1u.s; 4, Muntiacus reevesi; 5, Cervus nippon; 6, C . elaphus elaphus; 7 , C . e . c*anadensis; 8, Duma duma; 9, Axis axis; 10, Ranglfer tamndus: 1 l , Alces nlces alces; 12, A. a . gigcrs; 13, Mazamn spp. ; 14. Pudu pudu. Antler mass was calculated as gl(kg)' '"of lean weight in very large males. The exponent, 1.35, removes the effect of body size on deer from the same habitat and latitude, allowing a comparison of large- and small-bodied deer species. BMR, basal metabolic rate; 1 kcal = 4.1868 kJ.

to the minimum size of young. A species in a cold climate must bear large young to avoid hypothermia.

While antlers vary, so do hair and colour patterns of the coat (Fig. 17), but with a vital difference. Body colouration, the pattern of hair lengths, and the distribution of shade patterns appear to be due to hereditary factors with full penetrance. That is, they appear not to be subject to environmental variation. It is different for body and antler size and shape. Large mammals kept in zoos retain the external markings characteristic of their race, even though such environments differ greatly from natural ones.

The colouration of ruminant males appears to be organized

0 2 4 6 8 10

ANTLER MASS (g / (kg BODY WEIGHT)'^^)

FIG. 16. Percent milk solids correlated with relative antler mass. 1, Odocoileus ~irginicrnus; 2, 0 . hemionus; 3, Capreolus c.apreolus; 4. Cervus elaphus hipelaphus; 5 , C . e . cclnadensis; 6. Duma damn; 7, Rangifer tcrrandus; 8, Alee.\ crlces ale-ex; 9 , A. (1. nmericcrncr (Geist 1986~).

within what artists call "picture plans." That is, the breeding pelage of a male performing a dominance display appears to be characterized by attention-guiding mechanisms, which, in the same manner as the organization by artists of a picture plan on canvas, guide the observer's eye over the animal's body (Geist 1978a: pp. 90-98). The head and rear poles of the animals change synchronously (Fig. 17), a relationship pointed out by Portmann ( 1 959).

What is to be explained? Despite the apparent effect of environment on individual size

and porportions, there are genetic clines in the morphology of social organs and signals in some species. In others, no such clines exist. Both phenomena need explanations.

Since clines do exist, one must explain stasis in the evolution of social organs, showing also why some clines in social organs have no environmental correlates and why social and ecological adaptations appear to evolve independently. One must also explain how tissues of low growth priority (and highly sensitive to nutrition) become tissues of hi& growth priority (insensitive to nutrition) in evolutionary advancement.

Evolution through dispersal Clinal evolution in social organs of large mammals can be

explained as follows. ( I ) The evolution of novelty in social organs is a consequence

of explosive colonization and can occur if two conditions are met: (a) a parent population gives off colonizers at its periphery into a very large area of unoccupied, rich habitat so that the colonizers can disperse under conditions of great resource abundance; and (b) the colonizers expand geographically into zones of an increusingly longer productivity pulse.

Therefore, if there is no vacant, uncontested habitat or no increasing productivity pulse, there will be no speciation.

(2) Under the above conditions, a process is set in motion whereby first, the colonizers within three to four generations become full-fledged dispersal phenotypes; they grow

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CAN. J . ZOOL. VOL. 65, 1987

FIG. 18. A comparison of island and mainland forms of Rangifer from similar latitudes. Foreground, the Spitzbergen subspecies (R. rarandus platyrhynchus); background, barren-ground subspecies (R . r . groenlandicus). Note the short legs of the island form (de Bie et al. 1 977).

FIG. 17. Antler size covaries with the extent of other social organs so that large antler mass is associated with greater ornateness. (A) Rusa equina; (B) Rusa rimorensis. Note the differences in the size of antlers, in the neck mane, and in the size of the tail.

to maximum genetic body size and fully develop tissues of low growth priority or luxury tissues. In an uncontested, vacant habitat, such a development is permitted by superabundance of forage and selection by individuals of the most nutritious (high protein) forage.

(3) The population of dispersers has a gene pool differing from that of the parent population because of genetic drift during a population bottleneck.

(4) The colonizing dispersal phenotypes, surrounded by abun- dant material resources, switch from competition for material resources to severe social competition for high mating frequency.

(5) The colonizers have maximum reproductive rates because of the abundance of resources.

(6) Since full-fledged dispersal phenotypes grow to their maximum genetic potential, the differences in body size between individuals are now expected to be due to genetic differences. The genetic variance thus approaches unity and environmental variance approaches zero. Therefore the genetic basis for body size is fully exposed and rapid selection for body size can take place, if body size is adaptive.

(7) A vital factor in combat of ungulates is body size (Clutton- Brock et al. 1979).

(8) Since dispersal phenotypes are 2-5 times heavier than maintenance phenotypes and forces of collision roughly parallel body size, and because dispersal phenotypes in- teract socially very frequently, the bodies of males are

subjected frequently to severe strains and damage. This rapidly selects for sturdier skulls, hornlike organs, cervical vertebrae, and articulation surfaces. Organs of combat thus increase in sturdiness, along with body size.

(9) In ungulates, combat tends to be very damaging (Geist 1966, 197 la , 1978a, 1986d; Clutton-Brock 1982). We expect dispersal phenotype males to suffer high rates of combat damage, as is indicated by the severe damage of mouflon rams (Ovis ammon musimon) in a new colonizing population, heavily subsidized with artificial feeding (Ulenhaut and Stubbe 1980). From 180 skulls, 135 showed combat damage including healed fractures. Nothing like that is found in "normal" populations, that is, in populations of maintenance phenotypes.

(10) Dispersal phenotype males are expected to be generally short lived, because of the high cost of reproduction; females also should be short lived because of high reproduction (Williams 1957; Gadgil and Bossert 1970; Ellen- berg 1978; Patridge and Farquhar 198 1 ).

( 1 1) Granted high combat damage and short life expectancy, plus rapid selection for body size, then one generation of large males is quickly replaced by another of equal or larger size. This enhances social competition with each generation. There is evidence that body size may not increase gradually, but may increase by doubling (Lovtrup 1977: pp. 274-28 1).

(12) Under the above circumstances, bluffing becomes adaptive. Bluffing is the ability to convince an opponent to accept defeat without combat. It can be effective only if (a) opponents do not know one another, since for bluffing to work, the bluffing individual must hide his true ability to fight; and (6) the mating season is short, the population density is low, and the opponents roam widely during the mating season. That is, the chance of meeting a stranger is very high. Granted the above conditions (expected mainly during colonization), then males ought to become more choosy as to when to escalate an interaction into combat. Males should then benefit by any novelty effects, by en- hanced markings on the body that aid in apparently enlarg-

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FIG. 19. A comparison of (A) European and (B) American type moose. European moose carry a basic three-pronged, American moose, a four-pronged antler plan; each tine branches radially in the manner indicated to the right of the basic antler (on skull); outlined in black are the current record size antlers for each form. Outlined (left) beyond the record size antler of European moose is an antler from late Pleistocene - early Holocene moose found in bogs in East Prussia (today Poland, Kramer 1963). American type moose carry advanced, larger antlers, a larger bell, and have a more ornate, contrasting coat (Geist 1986b).

ing their body mass, and by intensifying colours associated with aggression. Novelty creates attention by being discre- pant, a subject investigated at length in psychology and other behavioural sciences (Geist 1978a: pp. 24-40).

(13) A novel effect is brought about as follows. Because of selection for body size, developmental instabilities arise, including phenodeviancy in markings. That is, selection for any one particular character is disruptive of normal development, including normal body markings (Belyaev 1979; Coppinger and Smith 1983). That could give the oddly marked large male an advantage in agonistic interac- tions with strangers in that novelty leads to arousal, being the obverse of predictability. Also, unidirectional selection, as well as the mating of incongruent genotypes in cross-breeding between somewhat different forms of the same species, fractions the established functional behavioural chains; this allows a reassembly of new behavioural chains via learning (Coppinger et al. 1987). Thus intense selection for size would generate not only raw materials for a new external appearance, but also for restructuring activities into new adaptive syndromes.

(14) With selection for large size, one expects, as a concom- itant of developmental instability, changes not only in gene frequency but also in the architecture of the chromosomes, and a rapid spread of chromosomal morphologies that rearranges genes to support large size. That is, the "dispersal pulse" that leads to severe selection for size should

generate great phenotypic variability. Great variability accompanied speciation in fishes and clams (Williamson 1981). There should be a change in chromosome architecture with latitudinal-altitudinal speciation; a change in chromosome numbers is observable (Nadler et al. 1974). Goldschmidt (1940) pointed out a similar phe- nomenon long ago.

(15) At maximum body size, differences in foraging ability between males express themselves in larger tissues of low growth priorities (luxury tissues). Such ornateness in the male (based on excesses of material resources beyond the demands of maintenance and body growth) can express itself in females as richer milk or larger young (Geist 1986~). Both factors would give the young a head start in growing large. Therefore, females should exercise a choice in favour of ornate males.

(16) If body size in males is adaptive, then it is adaptive in the female as well. Large females can bear larger young (Brody 1945) and spare a large fraction of ingested resources for milk production because of their relatively lower maintenance costs.

(17) Since dispersal into a habitat uninhabited by the colonizing species very likely confronts the colonizers with conditions and problems not encountered previously, there will be selection for dealing with novelty. There is, in the relatively short life-spans of individuals, a reproductive payoff in being able to evade novel dangers, or taking

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1078 CAN. J . ZOOL. VOL. 65, 1987

advantage of previously unexploited opportunities. It becomes adaptive to explore, to test, and to experiment. Under conditions of resource abundance, an individual can invest in experimentation and bear the cost of failure; under maintenance conditions (great resource shortages) the individual is best off reproductively to imitate proven (parental) solutions, which entail neither the cost of exploration nor the cost of failure. Consequently latitudinal- altitudinal evolution ought to be accompanied by evidence of broader abilities, greater learning abilities, and reduced reliance on instincts. We could expect, for instance, an increase in relative brain size within a lineage, which has been found between Tertiary and Pleistocene species (Thenius and Hofer 1960; Jerison 1961). The process of evolving novel ecological adaptations can only proceed where the costs of experimenting and failure are minimal, that is, under conditions of resource abundance. This im- plies that the evolution of novelty is most likely during explosive colonization of rich habitat. The dispersal- maintenance phenotype dichotomy also generates a barrier to gene flow: parental forms cannot compete socially against the larger-bodied descendants; the descendants, however, cannot maintain themselves on the meager resources of the parental range. The descendants are large- bodied, dispersal phenotypes, highly sensitive to nutrition- al shortages, so they leave in search of better forage (Geist 197 la) . Thus, colonizing individuals will most likely move outward into vacant habitat, not inward where resources have been depleted.

( 18) Colonization with intense social competition continues as long as resources are superabundant. The colonizing population, characterized by a very rapid turnover rate due to high reproductive output and short individual life expectancy, is ideal for the rapid spread of "winning" genetic combinations. Change in adaptations is assured the further the population colonizes terrain that is different from that of the parental population. When the land is colonized and resources begin to run short, there is a reversal towards maintenance phenotypes. However, the "new form" cannot shrink back to the size of its parent because of pro- longed genetic selection for large body size. With the reversal to maintenance phenotypes, efficiency selection takes over, fine tuning the new form during resource shortages brought on by population density, and in the long run, by the defensive coevolution of plants (Bryant and Kuropat 1980).

Efficiency selection increases ability to reproduce success- fully at less and less cost in parental maintenance, growth, and reproduction per offspring. It is a "fine tuning" of the adaptations acquired during explosive colonization. Efficiency selection improves adaptations to deal with resource shortages; it shapes the morphology of organs involved with finding, acquir- ing, and processing food, over long time spans. Gradual changes in tooth size and morphology are expected, such as increases in the size and hypsodonty of incisor teeth of the cave goat of Malorca, Myotragus (Azzaroli 1982), or cheek teeth of dwarfed island deer (Kuss 1975), African Suids (Cooke and Ewer 1972), and hippopotamuses (Coryndon 1978); changes in those skull parts that support a movable proboscis, as found in tapirs, oreodonts, and macrauchenids (Scott 1937); or the changes in those parts of the moose skull that support the enlarged movable nose, from the mid-Pleistocene Alces latifrons to Alces alces of recent times (Kurtkn 1968). One also

expects changes in skull shape resulting from chewing action that supports enlarged teeth, as possibly seen in mammoths over time (Stanley 1981: p. 15). In the absence of predation, one expects a deterioration in security adaptations, such as the reduction in appendages seen in the reindeer of Spitzbergen (Fig. 18) and in the cave goat Myotragus, or as has been noted in general in island forms of large mammals (Kuss 1975; Azzaroli 1982). The dwindling in size and restructuring of organs in island forms of large mammals may be an example of efficiency selection, allowed to go to extremes because of lack of predation.

We also expect luxury organs to shrink disproportionately with body size. Antler mass in European - West Siberian moose, which is about 60% that of American-type moose (Fig. 19), may have shrunk postglacially to its current value because late Pleistocene antlers of European moose are apparently quite large (Fig. 20). The dwarfing in horn size of Bison postglacially (Wilson 1980) may be another example, but it is not clear if this shrinking is disproportionate or not. Finally, we expect a shrink- age in brain size with efficiency selection on maintenance phenotypes, provided the range of adaptive activities is reduced, so that the diversih of tasks required to be mastered declines. This is because diversity of tasks mastered correlates with brain size (see review in Geist 1978u: pp. 3 1-32, 137- 140).

Efficiency selection would also manifest itself in vestigial organs, in that, over time, organs not effective in competition would be reduced as resources in growth are shifted to necessary organs. Examples are the loss of peripheral incisors and a concurrent enlargement of the remaining two central ones in Myotrugus (Azzaroli 1982) and the loss of canine teeth with enlargement of hornlike organs in cervids (Frick 1937). The loss of canines can be traced in the Alcini (Azzaroli 1981), the merycodontids and antilocaprids , the protoceratids (Frick 1937), and the rhinoceros (Thenius and Hofer 1960). It is also conceivable that teeth should shrink in size if other parts of the digestive system take up the process of forage degradation. Also, organs of securtiy should be subject to refinement; i.e., cursorial forms should, in their morphology, become increasingly more cursorial as evidenced by changes in body proportions associated with more efficient running. In the hippopotamuses of Africa, both the small (Hippopotamus liberien- sis) and the large forms (Hippopotamus amphibius) have de- veloped increasingly elevated orbits, as if to see better above the water (Coryndon 1978).

If dispersal and colonization from south to north and from small to large productivity pulses generate novel hypermorphs, then dispersal under obverse conditions (from north to south into a decreasing productivity pulse) should conserve primitiveness, should reduce body size and luxury organs, and under extreme conditions should generate paedomorphs and secondary primitiveness. Beringian mammals colonizing North America during and after megafaunal extinction follow that expectation. They also colonized under conditions of shrinking productivity pulses and local plant diversity (Guthrie 1984).

Because under maintenance conditions all individuals are relatively small and because body size is highly sensitive to material income, differences in body size now reflect almost exclusively environmental differences between individuals. Natural selection on body size, except under conditions of severe resource shortages, no longer affects the hereditary factors. That is, under "normal" conditions, when individuals are maintenance phenotypes, individual differences reflect environmental and not genetic differences. If, however, variation is

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GEIST 1079

FIG. 20. Size reductions in moose from (A) Alces latifrons, the broad-fronted moose of mid-Pleistocene Europe to (D) Alces alces cameloides, the extant dwarf moose of Manchuria. (B) Alces a . gigas, the largest extant moose. Note antler changes between (A) and (B). Cranial measurements indicate that the Alaskan moose is about half the body mass of the broad-fronted moose, and also has a more highly evolved rostrum. (C) The European type moose of today. The moose in (D) is about half the mass of the moose in (B) (Kahlke 1956a, 1956b; Kurt& 1968; Heptner et al. 196 1 ; Azzaroli 198 1 ).

largely environmental, natural selection becomes largely random with respect to the factor selected for. Under maintenance conditions, not much change is expected in social organs since the conditions for their evolution (resource abundance sparking intense social competition) are absent, while resource shortages shape individuals towards becoming conservative so as to minimize the loss of precious resourcis needed for reproduction. Thus evolution for both large body size and ornateness should come to a halt under maintenance conditions.

After a very rapid evolution of novelty in social organs there follows a period not of stasis, as stated by the punctuated equilibrium model, but of a slow, gradual (efficiency) restruc-

FIG. 21. Antler changes from early to late Pleistocene in Alces (A, B), Duma (C, D), Cervus elaphus (E, F ) , and the island deer Megaceros cretensis (G, H). Early Pleistocene forms at left, late Pleistocene - Holocene forms at right. In all cases the later forms have increased radial branching in the distal part of the antlers. Kuss (1975) considers M. cretensis as a new genus, Candiacervus, and does not accept the megacerine designation. (After Beninde 1937; Leonardi and Petronio 1976; Kuss 1975; Azzaroli 198 1 .)

turing. It is this phase, I suggest, one picks up in the fossil record, supporting the claim that gradual, long-term changes do occur in mammals (Gingerich 1980). In antlers of several cervid lineages one notes, for instance, a change from simple structured antlers to antlers with a more complex branching pattern, as well as a shift from the proximal to the distal portions of antlers (Fig. 21). It may be that simple antlers are of a morphology d.ictated by the brute force of large bodies, frequent combat, and rich resources, while complex antlers show the effects of efficiency selection and an emphasis on display (negotiations); social behaviour is cheap as shown by our heart-rate telemetry research on free-living bighorn sheep (MacArthur et al. 1982).

Some conclusions, predictions, and tests The dispersal theory of speciation agrees with the punctuated

model that speciation is episodic, real, and allopatric, and that it occurs in small, peripheral popultions. It predicts that the ear- liest members of a new species will be the largest and most diverse, and are likely to be accompanied by other species of large individual size and variability. Zoogeographically there will be a pattern of advanced forms with advanced forms, and primitives with primitives. Since explosive colonization is only likely after major climatic events, it predicts high rates of speciation in the Pleistocene with its many climatic pulses. Major climatic changes giving rise to colonization should give

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1080 CAN. J . ZOOL. VOL. 65, 1987

FIG. 22. The simplified, evolutionary model proposed shows rapid change in body size (and social organs) followed by a long-term, gradual (probably exponential) decline in body size as efficiency selection restructures the organism. At small body size, paedomorphic dwarfs may arise; they are the antithesis of the hypermorphic giants arising during the speciation event (after Geist 1 9 7 8 ~ ) .

rise simultaneously to many new species. Since speciation is tied to dispersal, one cannot expect to find the ancestral species with a descendent species in the same geographic area. Conse- quently new species appear seemingly out of "nowhere." However, if species evolve sympatrically via character dis- placement in closely related but incompatible lineages (Mayr 1966), then we do expect ancestor and decendent species in the same geographic area. Then species do not appear out of "nowhere" in the fossil record.

The dispersal theory agrees with the gradualistic model in that it predicts that there will be no stasis (Fig. 22), nor a steady mean about which character values will fluctuate. There will be a change in the evolutionary regime after speciation, but not stasis. The dispersal theory predicts slow, directional changes in character value generated by efficiency selection, as organs of food acquisition and processing and organs of security shift towards greater utility; it predicts vestigal organs, while social organs will change towards greater uniformity, and weapons towards greater display value. Efficiency evolution is likely to be rapid following speciation, but should decline with time, creating the appearance of stasis. Directional evolution, even in a steady state environment, is affirmed, but orthogenesis is denied.

Two trends are predicted. (i) The trend towards large body size (Cope's rule) as a consequence of colonization and concom- itant social selection. The more frequently a lineage colonizes and exploits new resources, the more species of large size it evolves, and the larger the giants. (ii) There will be increasing efficiency of organs as efficiency selection fine tunes a species via competition for material resources. Although gradualistic, the changes are not due to some internal property of organisms. Island species, for instance, in the absence of predation, are expected to decline into dwarfs with impaired security adaptations. They should be highly sensitive to extinction from mainland forms; they should have small social organs, but sophisti- cated food processing organs (Kuss 1975; Azzaroli 1982). Con- versely, severe predation should generate large-bodied dispersal

phenotypes, enhance security adaptations and luxury organs, and increase the chances of evolving novelty (because of the dispersal phenotype's disposition to explore). It can therefore be predicted that wide-roaming , roughage grazers from open landscapes, exposed to frequent contact with predators, are likely to frequently evolve large, ornate, cursorial forms, but are also more likely subject to extinction from specialization. This matches Vrba's (1980) findings on the paleontology of African antelope. Saltatorial hiders with small home ranges and catholic food habits are expected to speciate rarely, but to endure in geologic time. Hiding precludes full exploitation of resources in large open areas. An increase in predation pressure confines hiders (while it disperses cursorial forms); consequently predation shunts hiders towards the maintenance phenotype and thus conservatism, and curtails the evolution of novelty even during colonization. This explains in part why stenotopic forms speciate more frequently than eurytopic ones (Vrba 1980); the eurytopic Odocoileus is expected to be conservative in evolution with few species evolving, as has been found (Kurtkn and Anderson 1980), whereas the stenotopic megacerines should have evolved a plethora of short-lived species, as they did (Kurtkn 1968; Azzaroli 1979) (Fig. 23).

The dispersal theory also predicts four other directional changes in evolution: the evolution of hypermorphs and novelty with colonization of landscapes (or times) of increasing length of productivity pulse, and the evolution of paedomorphs and retention or regeneration of primitiveness with dispersal into a decreasing productivity pulse. An analysis of the fate of mammalian colonizers of North and South America would be instructive here.

While Darwinian evolution is affirmed, it is predicted that such evolution is very rare, because the ability of individuals to adjust protects the controller genes, let alone the structural genes, against natural selection. The greater the ability to deal with environmental contingencies, the less Darwinian evolution occurs. Therefore, protected epigenetically, changes in allele composition in the gene pool are expected to be mostly random in nature, and consequently constant in time. Speciation is not seen as a mere change in gene frequencies, but as a restructuring of chromosomal architecture as a consequence of severe social selection during colonization.

Fifteen years have passed since the dispersal hypothesis was first published (Geist 197 la , 197 16). How well have the explicit predictions published earlier (Geist 197 la: pp. 3 13-346) stood up? Attention by cytogeneticists, molecular biologists, but also paleontologists and zoogeographers to caprid evolution in the ensuing decade do allow an appraisal. The prediction that Ovia came from an Ammotragus-like ancester is now verified via chromosomes homologous in banding and fusion (Nadler et al. 1973, 1974), but also by the immunological closeness of Ammotragus, Capra, and Ovis (Hight and Nadler 1976). The prediction that the giant sheep (Ovis ammon) are a recent deriva- tive of urial stock (Ovis orientalis), while pachycerine sheep were an earlier, independent radiation was verified (Nadler et al. 1974). So was the prediction that the light-coloured eastern snow sheep with large rump patches (Ovis nivicola lydekkeri) could be due to a remigration of Beringian sheep into eastern Siberia as evidenced by their 2n = 52 karyotype compared with the 2n = 54 kasyotype for Dall's sheep (Ovis dalli), and their late Pleistocene fossil appearance (Korobitsyna et al. 1974). I proposed that large sheep evolved repeatedly; cytogeneticists identified three radiations (Nadler et ul. 1974), but there are likely a minimum for four (Geist 1985~) . That speciation in the

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FIG. 23. A sample of megacerine deer from mid and late Pleistocene. The stenotopic megacerines diversified into many short-lived species during about half a million years; the eurytopic Odocoileus hardly diversified at all during a span of time four times longer (Kurtbn and Anderson 1980). (A) Common fallow deer. Dama dama dama; (B) mid-Pleistocene fallow deer, D . d . clactonia; (C) Megaceros (Megaceroides) cretensis, small extinct island form, Kreta; (D) M. cerigensis, small extinct island form. Karpathos; (E) medium-sized, extinct island form, M. pigadiensis, Karpathos; (F) extinct island form, M. algarensis; (G) extant Mesapotamian fallow deer, D. d. me.sapotamica; (H) M veticornis, mid-Pleistocene; (1) M. solilhacus. mid-Pleistocene; (J) M. veticornis dendroceros, mid-Pleistocene; (K) M. (Megaceros) giganteus, late Pleistocene; (L) Sinomegaceros yabei, late Pleistocene, Japan; (M) M, savini, sympatric with M. veticornis, mid-Pleistocene. (After Kahlke 1956a. 1956b; Kuss 1975; Leonardi and Petronio 1976; Azzaroli 1979, 1982.)

Pleistocene was common has been verified by Gingerich ( 1977); rates of speciation and extinction rose fourfold over those in the Tertiary. That pachycerine sheep are fairly old, and that the centre of radial dispersion for bighorns was the Mojavl desert, emerged recently from an analysis of published and unpublished paleontological finds (see Geist 19856). A second centre of radial Pleistocene dispersal of bighorns has been identified in Wyoming.

The dispersal hypothesis, focussing on morphology, behaviour, and zoogeography, failed to identify the mouflon (Ovis musimon) as a recently evolved, evolutionary "throwback" or

paedomorphic dwarf. It did identify the mouflon as the most primitive sheep; cytogenetics identified it as derived from, not ancestral to, urials; paleontology identified a very late Pleis- tocene surge of mouflonlike sheep (Korobitsyna et al. 1974). This supported the cytogenetic analysis. By itself, none of the disciplines could have identified the mouflon as a paedomorphic dwarf. A second such dwarf, probably derived from a markhor- like goat (Capra), is very likely Pseudois. I considered it old, but although Pseudois are found in fossil deposits, their age is not established (Korobitsyna et al. 1974). Its karyotype is also 2n = 54, but is not homologous to that of mouflons (Bunch et al.

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1082 CAN. J . ZOOL. VOL. 65, 1987

1978). As expected, paedomorphic dwarfs from primitive sheep and goats ought to resemble one another closely, and they do.

A confusion of paedomorphic with primitive characters also occurred in my assessment of red deer (Geist 197 1 b). The Barbary stag (C. elaphus barbarus), with its paedomorphic features, is not the most primitive red deer; that honour goes to the Kashmir stag (C. e . afJinis) as suggested by Groves and Grubb (1 987).

It may be noted that distinct forms of sheep and goats arise together with a significant change in karyotype (Nadler et al. 1974), and subsequently diversify geographically into many "s~~bspecies." That is what Goldschmidt (1940) had found. He could not explain how rapid transformation into a new form could come about; the dispersal theory of speciation does show this.

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