The evolution of eutherian chromosomes

The gross organization of the genome of Eutheria (placental mammals) into chromosomes follows a simple architecture that, with some minor changes, is almost completely conserved for more than 100 million years in various species of almost all extant mammalian orders. Recent molecular cytogenetic results--especially those from the assumed oldest clade, the Afrotheria--suggest an ancestral karyotype that would calculate the "default" frequency of gross rearrangements to less than two changes within 10 million years of mammalian evolution. The main changes are the fission, movement and subsequent fusion of large chromosome segments or of chromosome arms. Reciprocal translocations are the exception. Chromosome numbers may have increased or decreased significantly in this fusion/fission process but, in most instances, the main architecture still remains evident. There are, however, some exceptions in mammals with extremely derived karyotypes.     

The evolution of viviparity within the Australian scincid lizardLerista bougainvillii

The semi-fossorial scincid lizard, Lerista bougainvillii , is oviparous throughout its extensive range in south-eastern mainland Australia. However, two widely separated (by approximately 1000 km) island populations are viviparous; in these populations the eggshell is lost and females retain their offspring in utero until embryogenesis complete. One mainland population in south-eastern Victoria shows an intermediate condition, in which the eggshells are incomplete and uterine embryogenesis is prolonged.
Morphological and electrophoretic analyses confirm a high degree of morphological and genetic similarity between populations (i.e. there is no evidence for the presence of more than one species), and phenetic analyses of these data show that each of the two disjunct viviparous populations more closely resembles adjacent oviparous populations than the other viviparous group. Hence, we infer that viviparity may have arisen twice within L. bougainvillii , in both cases on offshore islands with a cold climate.     

Intraspecific phylogeography of Lacerta vivipara and the evolution of viviparity

The lacertid lizard Lacerta vivipara is one of the few squamate species with two reproductive modes. We present the intraspecific phylogeny obtained from neighbor-joining and maximum-parsimony analyses of the mtDNA cytochrome b sequences for 15 individuals from Slovenian oviparous populations, 34 individuals from western oviparous populations of southern France and northern Spain, 92 specimens from European and Russian viviparous populations, and 3 specimens of the viviparous subspecies L. v. pannonica. The phylogeny indicates that the evolutionary transition from oviparity to viviparity probably occurred once in L. vivipara. The western oviparous group from Spain and southern France is phylogenetically most closely related to the viviparous clade. However, the biarmed W chromosome characterizing the western viviparous populations is an apomorphic character, whereas the uniarmed W chromosome, existing both in the western oviparous populations and in the geographically distant eastern viviparous populations, is a plesiomorphic character. This suggests an eastern origin of viviparity. Various estimates suggest that the oviparous and viviparous clades of L. vivipara split during the Pleistocene. Our results are discussed in the framework of general evolutionary models: the concept of an oviparity-viviparity continuum in squamates, the cold climate model of selection for viviparity in squamates, and the contraction-expansion of ranges in the Pleistocene resulting in allopatric differentiation.     

Reproduction and development ofSebastes in the context of the evolution of piscine viviparity

Synopsis Selected aspects of the reproduction and development ofSebastes and other rockfishes are reviewed in the context of piscine viviparity. Among the eight subfamilies of the Scorpaenidae, viviparity is confined to the subfamily Sebastinae; gestation is lumenal and the embryos usually develop to term within the egg envelope. Transitional states from oviparity to viviparity are evident in different species within the family. A scenario for the evolutionary origin of viviparity in rockfishes is derived from an analysis of scorpaeniform reproductive biology. Although viviparity is best developed in the genusSebastes, it is still in a primitive, unspecialized state. Rockfish viviparity is essentially lecithotrophic, i.e. embryonic nutrition is dependent on the energy reserves laid down during oogenesis. In other groups of viviparous fishes, lecithotrophy has been shown to be better suited energetically to seasonally unpredictable habitats, whereas matrotrophy requires a predictable food supply. During the evolution of an essentially primitive form of lecithotrophic viviparity in rockfishes, the advantages of high fecundity associated with oviparity were retained while an enormous increase in the survival rate of the developing embryos was acquired. The basic lecithotrophic pattern of oviparous development was not changed since it offered selective advantages both in terms of energetics and as a basis for retaining a large brood size.     

Potential targets for selection during the evolution of viviparity in cold-climate reptiles

Viviparity (live-bearing) has evolved from oviparity (egg-laying) in more than 100 lineages of squamate reptiles (lizards and snakes). This transition generally has occurred in cool climates, where thermal differentials between eggs in the (cool) nest versus the (warm) maternal oviduct influence embryonic development, in ways that may enhance offspring fitness. To identify specific traits potentially under selection, we incubated eggs of a montane scincid lizard at conditions simulating natural nests, maternal body temperatures, and an intermediate stage (2-week uterine retention of eggs prior to laying). Incubation at maternal temperatures throughout incubation affected the hatchling lizard’s activity level and boldness, as well as its developmental rate, morphology, and locomotor ability. A treatment that mimicked the initial stages of the transition toward viviparity had a major effect on some hatchling traits (locomotor speeds), a minor effect on others (tail length, total incubation period) and no effect on yet others (offspring behaviors). More generally, different aspects of the phenotype are sensitive to incubation conditions at different stages of development; thus, the evolution of reptilian viviparity may have been driven by a succession of advantages that accrued at different stages of embryogenesis.     

Mammalian viviparity: a complex niche in the evolution of genomic imprinting

Evolution of mammalian reproductive success has witnessed a strong dependence on maternal resources through placental in utero development. Genomic imprinting, which has an active role in mammalian viviparity, also reveals a biased role for matrilineal DNA in its regulation. The co-existence of three matrilineal generations as one (mother, foetus and post-meiotic oocytes) has provided a maternal niche for transgenerational co-adaptive selection pressures to operate. In utero foetal growth has required increased maternal feeding in advance of foetal energetic demands; the mammary glands are primed for milk production in advance of birth, while the maternal hypothalamus is hormonally primed by the foetal placenta for nest building and post-natal care. Such biological forward planning resulted from maternal–foetal co-adaptation facilitated by co-expression of the same imprinted allele in the developing hypothalamus and placenta. This co-expression is concurrent with the placenta interacting with the adult maternal hypothalamus thereby providing a transgenerational template on which selection pressures may operate ensuring optimal maternalism in this and the next generation. Invasive placentation has further required the maternal immune system to adapt and positively respond to the foetal allotype. Pivotal to these mammalian evolutionary developments, genomic imprinting emerged as a monoallelic gene dosage regulatory mechanism of tightly interconnected gene networks providing developmental genetic stability for in utero development.     

Low oxygen: a constraint on the evolution of viviparity in reptiles

The evolution of reptilian viviparity (live bearing) from oviparity (egg laying) is thought to require transitional stages of increasingly longer periods of embryonic development in utero, that is, longer periods of egg retention by the gravid female. Studies on sceloporine lizards demonstrate that embryonic responses to egg retention that is extended beyond the time of normal oviposition range from developmental arrest to normal development. The present study was designed to test the hypothesis that O(2) availability is the proximate factor that determines the rate and degree of development that reptilian embryos undergo in utero. Eggs of Sceloporus undulatus were incubated under conditions of low (LOX), normal (NOX), and high (HOX) oxygen both early and late in development. The LOX treatment consistently had a negative effect on development in terms of embryonic differentiation and growth, length of incubation, egg mortality, and hatchling size. Moreover, the LOX treatment had a stronger negative effect later in development than earlier in development. The results support the hypothesis that limited oxygen availability in utero acts as a developmental constraint. They further indicate that selection for extended egg retention, per se, will not lead to viviparity unless each incremental increase in the duration of egg retention is coupled with selection for traits (e.g., vascularity of oviduct and chorioallantois, hemoglobin oxygen affinity, etc.) that enhance O(2) availability to embryos. Such selection would be the most efficacious in cold climates where the effects of hypoxia would be the least likely to limit embryonic development.     

Time scale of eutherian evolution estimated without assuming a constant rate of molecular evolution

Controversies over the molecular clock hypothesis were reviewed. Since it is evident that the molecular clock does not hold in an exact sense, accounting for evolution of the rate of molecular evolution is a prerequisite when estimating divergence times with molecular sequences. Recently proposed statistical methods that account for this rate variation are overviewed and one of these procedures is applied to the mitochondrial protein sequences and to the nuclear gene sequences from many mammalian species in order to estimate the time scale of eutherian evolution. This Bayesian method not only takes account of the variation of molecular evolutionary rate among lineages and among genes, but it also incorporates fossil evidence via constraints on node times. With denser taxonomic sampling and a more realistic model of molecular evolution, this Bayesian approach is expected to increase the accuracy of divergence time estimates.     

Supertree analyses of the roles of viviparity and habitat in the evolution of atherinomorph fishes

Using supertree phylogenetic reconstructions, we investigate how livebearing and freshwater adaptations may have shaped evolutionary patterns in the Atherinomorpha, a large clade (approximately 1500 extant species) of ray-finned fishes. Based on maximum parsimony reconstructions, livebearing appears to have evolved at least four times independently in this group, and no reversions to the ancestral state of oviparity were evident. With respect to habitat, at least five evolutionary transitions apparently occurred from freshwater to marine environments, at least two transitions in the opposite direction, and no clear ancestral state was identifiable. All viviparous clades exhibited more extant species than their oviparous sister taxa, suggesting that transitions to viviparity may be associated with cladogenetic diversification. Transitions to freshwater were usually, but not invariably associated with increased species richness, but the trend was, overall, not significant among sister clades. Additionally, we investigated whether livebearing and freshwater adaptations are currently associated with elevated risks of extinction as implied by species' presence on the 2004 IUCN Red List. Despite being correlated with decreased brood size, livebearing has not significantly increased extinction risk in the Atherinomorpha. However, freshwater species were significantly more likely than marine species to be listed as endangered.     

Influence of the evolution of viviparity on eggshell morphology in the lizard Lerista bougainvillii

In reptiles, the evolutionary transition from egg-laying to live-bearing is thought to involve a gradual increase in the duration of egg retention, with progressively more development occurring prior to oviposition, and culminating in the birth of fully developed offspring. However, prolonging the retention of fully-shelled eggs within the oviducts may pose serious gas-exchange problems for the embryos. Thus, evolutionary increases in the period of intrauterine retention may require correlated decreases in the thickness of eggshells and/or their degree of calcification to allow for adequate embryonic gas exchange. To test this evolutionary model, eggs of three distinct reproductive forms of the scincid lizard Lerista bougainvillii were examined to determine the evolutionary relationships between the thickness of the shell membrane, degree of eggshell calcification, and the duration of uterine egg retention. These comparisons revealed the predicted pattern of correlated shifts in eggshell morphology and embryonic stage at oviposition. Evolutionary increases in the duration of egg retention were accompanied by decreases in the thickness of the eggshell membrane and degree of eggshell calcification. This evolutionary model suggests that there may be a tradeoff between the advantages of extended egg retention and the disadvantages of a thinner eggshell. On the basis of this tradeoff, I propose that oviparous taxa with relatively thin eggshells may be preadapted to evolve viviparity. Comparative examination of the limited data available on eggshell thickness in lizards supports this possibility. © 1996 Wiley-Liss, Inc.     

An empirical test of the `predictability' hypothesis for the evolution of viviparity in reptiles

Abstract Viviparity (live‐bearing) has evolved from oviparity (egg‐laying) >100 times in reptile phylogeny, but the selective forces responsible remain unclear. Tinkle & Gibbons (1977) proposed that prolonged uterine retention of eggs (leading ultimately to viviparity) is favoured by natural selection when it allows the reproducing female to better predict the incubation conditions that will occur in alternative potential nest‐sites, and hence select the optimal site in which to deposit her eggs. This ingenious hypothesis has never been tested empirically. Over a 7‐year period, I monitored temperatures inside 124 natural nests of egg‐laying scincid lizards at three different elevations in the Brindabella Range of south‐eastern Australia. As a measure of thermal predictability, I used correlation coefficients from comparisons of temperatures early vs. later in incubation among nests within each site. Both the mean and standard deviation of nest temperatures were examined in this way for each week through incubation. I performed these calculations under two models: one where the female assesses nest temperatures at the time of oviposition only, and one where she monitors temperatures constantly from the usual oviposition date until the actual time of laying. These analyses falsified two major assumptions of the ‘predictability’ hypothesis. First, nest temperatures at higher elevations were no less predictable than were those at lower elevations; instead, predictability was high in all situations. Secondly, a longer delay before oviposition decreased rather than increased the predictability of thermal conditions during subsequent incubation. I conclude that critical assumptions of the ‘predictability’ hypothesis are not supported in this study system.     

Evolution of viviparity: variation between two sceloporine lizards in the ability to extend egg retention

The evolutionary transition between oviparity and viviparity in squamate reptiles presumably occurs via a gradual increase in the duration of egg retention, the production of thinner eggshells, and increases in the vascularity of maternal and embryonic tissues. The 'ease' of this transition may differ among taxa. For example, in the genus Sceloporus , the scalaris species group contains both oviparous and viviparous species, and female Sceloporus scalaris can extend egg retention facultatively in response to the absence of a suitable site for oviposition without impairing embryonic development. In contrast, the undulatus species group contains only oviparous species, and, while female Sceloporus virgatus can extend egg retention, doing so retards embryonic development. I tested several hypotheses that would explain the greater ability of 5. scalaris than S. virgatus to extend egg retention. In this study, female S. scalaris retained eggs for 19 d without affecting the mortality of embryos, total developmental time, or dry mass of hatchlings. In contrast, when female S. virgatus retained eggs for 18 d, embryos had very high mortality and eggs took significantly longer to hatch than control (non-retained) eggs, although the dry mass of hatchlings was not affected. The ability of S. scalaris females to retain eggs with little negative effect on embryonic development was associated with relatively large chorioallantois, relatively thin eggshells, and relatively small clutch masses. These observations suggest that phylogenetic differences in the ability to extend egg retention may facilitate or constrain the evolution of viviparity in some lineages.     

The evolution of egg size in the brood parasitic cuckoos

We compared genera of nonparasitic cuckoos and two groups ofparasitic cuckoos: those raised together with host young ("nonejectors")and those in which the newly hatched cuckoo either ejects thehost eggs or chicks, or kills the host young ("ejectors"). Nonejectorsare similar to their hosts in body size and parasitize largerhosts than do ejectors, which parasitize hosts much smallerthan themselves. In both types of parasite, the cuckoo's eggtends to match the host eggs in size. To achieve this, nonejectorshave evolved a smaller egg for their body size than have nonparasiticcuckoos, and ejectors have evolved an even smaller egg. Amongejector cuckoo genera, larger cuckoos have larger eggs relativeto the eggs of their hosts, and the relationship between cuckooegg volume (mass of the newly-hatched cuckoo) and host egg volume(mass to be ejected) did not differ from that predicted by weight-liftingallometry. However, comparing among Cuculus cuckoo species,the allometric slope differed from the predicted, so it is notclear that egg size is related to the need to give the cuckoochick sufficient strength for ejection. Comparing the two mostspeciose ejector genera, Chrysococcyx cuckoos (smaller and parasitizedome-nesting hosts) lay eggs more similar in size to their host'seggs than do Cuculus cuckoos (larger and parasitize open cup–nestinghosts). Closer size-matching of host eggs in Chrysococcyx mayreflect the following: (1) selection to reduce adult body massto facilitate entry through small domed nest holes to lay, and(2) less need for a large egg, because longer incubation periodsin dome-nesting hosts allow the young cuckoo more time to growbefore it need eject host eggs.     

The origin of eutherian mammals

Palaeontologically recognizable eutherians originated no later than the Early Cretaceous in warm, probably moderately seasonal climates. Immediate ancestors were small, sharing many anatomical, physiological and reproductive features with small modern marsupials. Development of characteristically eutherian features involved interactions of body size, rates of metabolism, energetic costs of reproduction, anatomical/physiological processes of development and effects of each upon rates of population growth. In contrast to eutherians, marsupials have a narrow range of basal metabolic rates (lacking high rates), and show no direct links between rate of energy expenditure and gestation period, postnatal growth rate, fecundity or reproductive potential. Biological implications of this contrast are most pronounced at small body sizes. When resources are abundant, the relatively higher growth rates and earlier maturation of small eutherians (particularly those with high rates of metabolism) can lead to rapid population growth; among most marsupials, however, both pre- and postnatal constraints apparently preclude attainment of such high rates of reproduction. Also, only eutherians among the amniotes combine intimacy of placentation with prolonged active intra-uterine morphogenesis. Once established, that combination permitted (and even favoured) increases in diversity of adaptation in such disparate aspects as elevated metabolic rate, increased pre- and postnatal growth rates, increased encephalization, greater longevity, increased gregariousness, greater karyotypic flexibility, and augmented variability in adult morphology. However, all such boosts in diversity were probably secondary and dependent upon prior innovation of trophoblastic/uterine wall immunological protection of foetal tissues during prolonged intra-uterine development. Increased metabolic rates followed thereafter, with synergisms that may have speeded evolution among early eutherians. Eutherian-style trophoblast probably originated in the Mesozoic. Dependent adaptations, variably expressed, evolved later in sundry descendant lineages. Reproductive differences between marsupials and eutherians are not biologically trivial; to the contrary, breakthroughs among eutherians assured their dominance: (1) in high intensity food habits; (2) at small body masses; and (3) in very cold climates.     

The distribution of eutherian body weights

Summary The frequency distributions of eutherian body weights given by Caughley and Krebs (1983) are here corrected for an algebraic error in that publication. The distributions for hervibores and omnivores combined and for carnivores and insectivores combined are bimodal, the trough for the first group lying between 25 and 35 kg and for the second between 0.1 and 0.3 kg. The trough within the distribution of weights for herbivores and omnivores combined has been suggested (Caughley and Krebs 1983) as dividing those species whose populations are regulated intrinsically from the larger species whose populations are regulated extrinsically.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

Indel evolution of mammalian introns and the utility of non-coding nuclear markers in eutherian phylogenetics

Nuclear DNA intron sequences are increasingly used to investigate evolutionary relationships among closely related organisms. The phylogenetic usefulness of intron sequences at higher taxonomic levels has, however, not been firmly established and very few studies have used these markers to address evolutionary questions above the family level. In addition, the mechanisms driving intron evolution are not well understood. We compared DNA sequence data derived from three presumably independently segregating introns (THY, PRKC I and MGF) across 158 mammalian species. All currently recognized extant eutherian mammalian orders were included with the exception of Cingulata, Dermoptera and Scandentia. The total aligned length of the data was 6366 base pairs (bp); after the exclusion of autapomorphic insertions, 1511 bp were analyzed. In many instances the Bayesian and parsimony analyses were complementary and gave significant posterior probability and bootstrap support (>80) for the monophyly of Afrotheria, Euarchontoglires, Laurasiatheria and Boreoeutheria. Apart from finding congruent support when using these methods, the intron data also provided several indels longer than 3 bp that support, among others, the monophyly of Afrotheria, Paenungulata, Ferae and Boreoeutheria. A quantitative analysis of insertions and deletions suggested that there was a 75% bias towards deletions. The average insertion size in the mammalian data set was 16.49 bp +/- 57.70 while the average deletion was much smaller (4.47 bp +/- 14.17). The tendency towards large insertions and small deletions is highlighted by the observation that out of a total of 17 indels larger than 100 bp, 15 were insertions. The majority of indels (>60% of all events) were 1 or 2 bp changes. Although the average overall indel substitution rate of 0.00559 per site is comparable to that previously reported for rodents and primates, individual analyses among different evolutionary lineages provide evidence for differences in the formation rate of indels among the different mammalian groups.