Fetal nutrition in lecithotrophic squamate reptiles: Toward a comprehensive model for evolution of viviparity and placentation

The primary pattern of embryonic nutrition for squamate reptiles is lecithotrophy; with few exceptions, all squamate embryos mobilize nutrients from yolk. The evolution of viviparity presents an opportunity for an additional source of embryonic nutrition through delivery of uterine secretions, or placentotrophy. This pattern of embryonic nutrition is thought to evolve through placental supplementation of lecithotrophy, followed by increasing dependence on placentotrophy. This review analyzes the relationship between reproductive mode and pattern of embryonic nutrition in three lecithotrophic viviparous species, and oviparous counterparts, for concordance with a current model for the evolution of viviparity and placentation. The assumptions of the model, that nutrients for oviparous embryos are mobilized from yolk, and that this source is not disrupted in the transition to viviparity, are supported for most nutrients. In contrast, calcium, an essential nutrient for embryonic development, is mobilized from both yolk and eggshell by oviparous embryos and reduction of eggshell calcium is correlated with viviparity. If embryonic fitness is compromised by disruption of a primary source of calcium, selection may not favor evolution of viviparity, yet viviparity has arisen independently in numerous squamate lineages. Studies of fetal nutrition in reproductively bimodal species suggest a resolution to this paradox. If uterine calcium secretion occurs during prolonged intrauterine egg retention, calcium placentotrophy evolves prior to viviparity as a replacement for eggshell calcium and embryonic nutrition will not be compromised. This hypothesis is integrated into the current model for evolution of viviparity and placentation to address the unique attributes of calcium nutrition. The sequence of events requires a shift in timing of uterine calcium secretion and the embryonic mechanism of calcium retrieval to be responsive to calcium availability. Regulation of uterine calcium secretion and the mechanism of embryonic uptake of calcium are important elements to understanding evolution of viviparity and placentation. J. Morphol., 2013. © 2013 Wiley Periodicals, Inc.     

Evolution of placentation among squamate reptiles: recent research and future directions

Squamate reptiles are uniquely suited to study of evolution of reproductive mode and pattern of embryonic nutrition. Viviparous species have evolved from oviparous ancestors on numerous occasions, patterns of nutritional provision to embryos range widely from lecithotrophy, at one end of a continuum, to placentotrophy at the other, and structure and function of the maternal-embryonic relationship is highly constrained resulting in parallel evolutionary trajectories among taxa. Embryos of oviparous species primarily receive nourishment from yolk, but also mobilize a significant quantity of calcium from the eggshell. Most viviparous species also are predominantly lecithotrophic, yet all viviparous species are placentotrophic to some degree. Similarities in embryonic development and nutritional pattern between oviparous species and most viviparous species suggest that the pattern of nutrition of oviparous squamates is an exaptation for the evolution of viviparity and that placentotrophy and viviparity evolve concomitantly. The few species of squamates that rely substantially on placentotrophy have structural modifications of the interface between the embryo and mother that are interpreted as adaptations to enhance nutritional exchange. Recent studies have extended understanding of the diversity of embryonic nutrition and placental structure and have resulted in hypotheses for transitions in the evolution of placentotrophy, yet data are available for few species. Indirect tests of these hypotheses, by comparison of structural-functional relationships among clades in which viviparity has evolved, awaits further study of the reproductive biology of squamates.     

Vertebral evolution and the diversification of squamate reptiles

Taxonomic, morphological, and functional diversity are often discordant and independent components of diversity. A fundamental and largely unanswered question in evolutionary biology is why some clades diversify primarily in some of these components and not others. Dramatic variation in trunk vertebral numbers (14 to >300) among squamate reptiles coincides with different body shapes, and snake-like body shapes have evolved numerous times. However, whether increased evolutionary rates or numbers of vertebrae underlie body shape and taxonomic diversification is unknown. Using a supertree of squamates including 1375 species, and corresponding vertebral and body shape data, we show that increased rates of evolution in vertebral numbers have coincided with increased rates and disparity in body shape evolution, but not changes in rates of taxonomic diversification. We also show that the evolution of many vertebrae has not spurred or inhibited body shape or taxonomic diversification, suggesting that increased vertebral number is not a key innovation. Our findings demonstrate that lineage attributes such as the relaxation of constraints on vertebral number can facilitate the evolution of novel body shapes, but that different factors are responsible for body shape and taxonomic diversification.     

Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes)

Climate may play important roles in speciation, such as causing the range fragmentation that underlies allopatric speciation (through niche conservatism) or driving divergence of parapatric populations along climatic gradients (through niche divergence). Here, we developed new methods to test the frequency of climate niche conservatism and divergence in speciation, and applied it to species pairs of squamate reptiles (lizards and snakes). We used a large‐scale phylogeny to identify 242 sister species pairs for analysis. From these, we selected all terrestrial allopatric pairs with sufficient occurrence records (n = 49 pairs) and inferred whether each originated via climatic niche conservatism or climatic niche divergence. Among the 242 pairs, allopatric pairs were most common (41.3%), rather than parapatric (19.4%), partially sympatric (17.7%), or fully sympatric species pairs (21.5%). Among the 49 selected allopatric pairs, most appeared to have originated via climatic niche divergence (61–76%, depending on the details of the methods). Surprisingly, we found greater climatic niche divergence between allopatric sister species than between parapatric pairs, even after correcting for geographic distance. We also found that niche divergence did not increase with time, further implicating niche divergence in driving lineage splitting. Overall, our results suggest that climatic niche divergence may often play an important role in allopatric speciation, and the methodology developed here can be used to address the generality of these findings in other organisms.     

Speciation in Darwin's darklings: taxonomy and evolution of Stomion beetles in the Galápagos Islands, Ecuador (Insecta: Coleoptera: Tenebrionidae)

Stomion is one of three speciose and taxonomically difficult genera of flightless Darwin's darkling beetles of the Galápagos Islands. The previously named species and subspecies of Stomion are analysed by morphometric and cladistic methods. Eleven species are here recognized, which probably descended from colonization by a single ancestral species. Cladistic analysis yielded two weakly supported clades that are different from previously published morphological and allozyme genotype groups. Phenotypic and genotypic characters may be evolving independently. There is much within-species variation, but there is no compelling evidence of adaptive radiation in Stomion , in contrast to that in the famous Darwin's finches. The analyses show the need for changes in morpho-species taxonomy: S. punctipennis Van Dyke ( syn. nov. ) is elevated to full species from a subspecies of S. galapagoensis Waterhouse. There is no evidence to support the validity of: S. laevigatum santacruzensi Franz ( syn. nov. ), synonomized here under S. l. laevigatum Waterhouse; S. galapagoensis leleupi Kaszab ( syn. nov. ), synonomized here under S. linelli Blair; S. galapagoensis pinzoni Franz ( syn. nov. ), synonomized here under S. obesum Van Dyke. S. genovesa sp. nov. is described from Genovesa Island. Lectotypes are designated for S. galapagoensis Waterhouse, S. laevigatum Waterhouse and S. helopoides Waterhouse .   © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 141 , 135–152.     

Molecular systematics of neotropical cat-eyed snakes: a test of the monophyly of Leptodeirini (Colubridae: Dipsadinae) with implications for character evolution and biogeography

The Leptodeirini has been presumed to be a monophyletic assemblage based on albumin immunological data and morphology and consisted of neotropical cat-eyed snakes ( Leptodeira ), blunt-headed vine snakes ( Imantodes ), nightsnakes ( Eridiphas , Hypsiglena , and Pseudoleptodeira ), and the cloud forest snake ( Cryophis ). In the present study, approximately 1.4 kb of mitochondrial DNA sequence data (from cob and nad4 ) were collected to test the monophyly of the Leptodeirini. These data were analysed using maximum parsimony, maximum likelihood, and Bayesian methods. None of the results supported the monophyly of the Leptodeirini. There was strong support for a clade containing Imantodes and Leptodeira , and another clade containing the nightsnakes, with the latter placed closer to Cryophis and other dipsadine genera ( Sibon , Dipsas , and Atractus ). This partial reassessment of the Dipsadinae infers the group to have an ancestral condition of being rear-fanged, mildly venomous, and feeding on ectothermal vertebrates, with a more derived radiation that has lost the rear-fanged, venomous condition and has a diet specialized on invertebrates. A brief discussion on the biogeography of the dipsadines shows the group to be much older (Palaeocene), consistent with earlier views, as opposed to a more recent (Miocene) hypothesis, as has been recently suggested.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 483–500.     

Morphology, development, and evolution of fetal membranes and placentation in squamate reptiles

Current studies on fetal membranes of reptiles are providing insight into three major historical transformations: evolution of the amniote egg, evolution of viviparity, and evolution of placentotrophy. Squamates (lizards and snakes) are ideal for such studies because their fetal membranes sustain embryos in oviparous species and contribute to placentas in viviparous species. Ultrastructure of the fetal membranes in oviparous corn snakes (Pituophis guttatus) shows that the chorioallantois is specialized for gas exchange and the omphalopleure, for water absorption. Transmission and scanning electron microscopic studies of viviparous thamnophine snakes (Thamnophis, Storeria) have revealed morphological specializations for gas exchange and absorption in the intra-uterine environment that represent modifications of features found in oviparous species. Thus, fetal membranes in oviparous species show morphological differentiation for distinct functions that have been recruited and enhanced under viviparous conditions. The ultimate in specialization of fetal membranes is found in viviparous skinks of South America (Mabuya) and Africa (Trachylepis, Eumecia), in which placentotrophy accounts for nearly all of the nutrients for development. Ongoing research on these lizards has revealed morphological specializations of the chorioallantoic placenta through which nutrient transfer is accomplished. In addition, African Trachylepis show an invasive form of implantation, in which uterine epithelium is replaced by invading chorionic cells. Ongoing analysis of these lizards shows how integration of multiple lines of evidence can provide insight into the evolution of developmental and reproductive specializations once thought to be confined to eutherian mammals.     

Suprageneric relationships of galliform birds (Aves, Galliformes): a cladistic analysis of morphological characters

Of the basal clades of extant birds (Neornithes) the 'landfowl' or galliforms (Aves, Galliformes) are the most speciose. Cladistic analysis of more than 100 morphological characters coded at the generic level for most putative galliform genera confirms that the megapodes ('mound builders'; Megapodiidae) are the most basal clade within the order. They are followed successively by the curassows, guans and chachalacas (Cracidae), which comprise the sister-group to all other extant Galliformes (i.e. Phasianoidea). Within this large 'phasianoid' clade, analyses suggest that the guineafowl (Numididae) are the most basal taxon, although monophyly of this 'family' is not strictly supported on the basis of the morphological characters employed. An additional major clade within the phasianoid Galliformes is recovered by this analysis, comprising the traditional groupings of New World quails (Odontophoridae) and Old World quails ('Perdicini'), yet only monophyly of the former is supported unambiguously by morphological characters. Relationships within the remainder of the phasianoid taxa, including the grouse (Tetraonidae), turkeys (i.e. Meleagris / Agriocharus spp.) as well as other 'pavonine' galliforms (i.e. peafowl; Pavo , Afropavo , Rheinardia , Argusianus and Polyplectron spp.) remain largely unresolved on the basis of morphological characters, yet monophyly of the major subdivisions is supported here. Although there are a number of important differences, especially with regard to relationships within the nonquail phasianoids, the results of this morphological phylogenetic (cladistic) analysis are broadly congruent both with traditional classifications and existing molecular hypotheses of galliform phylogenetic relationships.     

Group living in squamate reptiles: a review of evidence for stable aggregations

How sociality evolves and is maintained remains a key question in evolutionary biology. Most studies to date have focused on insects, birds, and mammals but data from a wider range of taxonomic groups are essential to identify general patterns and processes. The extent of social behaviour among squamate reptiles is under‐appreciated, yet they are a promising group for further studies. Living in aggregations is posited as an important step in the evolution of more complex sociality. We review data on aggregations among squamates and find evidence for some form of aggregations in 94 species across 22 families. Of these, 18 species across 7 families exhibited ‘stable’ aggregations that entail overlapping home ranges and stable membership in long‐term (years) or seasonal aggregations. Phylogenetic analysis suggests that stable aggregations have evolved multiple times in squamates. We: (i) identify significant gaps in our understanding; (ii) outline key traits which should be the focus of future research; and (iii) outline the potential for utilising reproductive skew theory to provide insights into squamate sociality.     

Phylogeny of the Platyhelminthes and the evolution of parasitism

Robust phylogenies provide the basis for interpreting biological variation in the light of evolution. Homologous features provide phylogenetically informative characters whereas homoplasious characters provide phylogenetic noise. Both provide evolutionary signal. We have constructed molecular and morphologically based phylogenies of the phylum Platyhelminthes using a recently revised morphological character matrix and complete 18S and two partial 28S rRNA gene sequences in order to evaluate the emergence and subsequent divergence of parasitic forms. In total we examine 65 morphological characters, 97 18S rDNA, 41 Dl domain 28S rDNA, and 49 D3-D6 domain 28S rDNA sequences. For the molecular data there were 748, 132 and 249 phylogenetically informative sites for the 18S, Dl and D3-D6 28S rDNA data sets respectively. Morphological and molecular phylogenetic solutions are incongruent but not incompatible, and using the principles of conditional combination (18S rDNA + morphology passing Templeton's test) they demonstrate: a single and relatively early origin for the parasitic Neodermata (including the cestodes, trematodes and monogeneans); sister-group status between the cestodes and monogeneans, and between these taxa and the trematodes (digeneans and aspidogastreans). The sister-group to the Neodermata is likely to be a large clade of neoophoran turbellarians, based on combined evidence, or a clade consisting of the Fecampiid + Urastomid turbellarians, based on morphological evidence alone. The combined evidence solution for the phylogeny of fiatworms based on 18S rDNA and morphology is used to interpret morphological and life-history data and to support a model for the evolution and radiation of neodermatan parasites in the group.     

Correlated evolution between targets of pre‐ and postcopulatory sexual selection across squamate reptiles

Sexual selection reflects the joint contributions of precopulatory selection, which arises from variance in mating success, and postcopulatory selection, which arises from variance in fertilization success. The relative importance of each episode of selection is variable among species, and comparative evidence suggests that traits targeted by precopulatory selection often covary in expression with those targeted by postcopulatory selection when assessed across species, although the strength and direction of this association varies considerably among taxa. We tested for correlated evolution between targets of pre‐ and postcopulatory selection using data on sexual size dimorphism (SSD) and testis size from 151 species of squamate reptiles (120 lizards, 31 snakes). In squamates, male–male competition for mating opportunities often favors large body size, such that the degree of male‐biased SSD is associated with the intensity of precopulatory selection. Likewise, competition for fertilization often favors increased sperm production, such that testis size (relative to body size) is associated with the intensity of postcopulatory selection. Using both conventional and phylogenetically based analyses, we show that testis size consistently decreases as the degree of male‐biased SSD increases across lizards and snakes. This evolutionary pattern suggests that strong precopulatory selection may often constrain the opportunity for postcopulatory selection and that the relative importance of each selective episode may determine the optimal resolution of energy allocation trade‐offs between traits subject to each form of sexual selection.     

Vicariance and endemism in a Neotropical savanna hotspot: distribution patterns of Cerrado squamate reptiles

Aim To test predictions of the vicariance model, to define basic biogeographical units for Cerrado squamates, and to discuss previous biogeographical hypotheses. Location Cerrado; South American savannas south of the Amazon, extending across central Brazil, with marginal areas in Bolivia and Paraguay and isolated relictual enclaves in adjacent regions. Methods We compiled species occurrence records via field sampling and revision of museum specimens and taxonomic literature. All species were mapped according to georeferenced locality records, and classified as (1) endemic or non‐endemic, (2) typical of plateaus or depressions, and (3) typical of open or forested habitats. We tested predictions of the vicariance model using biotic element analysis, searching for non‐random clusters of species ranges. Spatial congruence of biotic elements was compared with putative areas of endemism revealed by sympatric restricted‐range species. Effects of topographical and vegetational mosaics on distribution patterns were studied according to species composition in biotic elements and areas of endemism. Results We recorded 267 Cerrado squamates, of which 103 (39%) are endemics, including 20 amphisbaenians (61% endemism), 32 lizards (42%) and 51 snakes (32%). Distribution patterns corroborated predictions of the vicariance model, revealing groups of species with significantly clustered ranges. An analysis of endemic species recovered seven biotic elements, corroborating results including non‐endemics. Sympatric restricted‐range taxa delimited 10 putative areas of endemism, largely coincident with core areas of biotic elements detected with endemic taxa. Distribution patterns were associated with major topographical and vegetational divisions of the Cerrado. Endemism prevailed in open, elevated plateaus, whereas faunal interchange, mostly associated with forest habitats, was more common in peripheral depressions. Main conclusions Our results indicate that vicariant speciation has strongly shaped Cerrado squamate diversity, in contrast to earlier studies emphasizing faunal interchange and low endemism in the Cerrado vertebrate fauna. Levels of squamate endemism are higher than in any other Cerrado vertebrate group. The high number of recovered endemics revealed previously undetected areas of evolutionary relevance, indicating that biogeographical patterns in the Cerrado were poorly represented in previous analyses. Although still largely undocumented, effects of vicariant speciation may be prevalent in a large fraction of Cerrado and Neotropical biodiversity.     

A family of short retroposons (Squam1) from squamate reptiles (Reptilia: Squamata): Structure,evolution, and correlation with phylogeny

Sequences of the SINE family specific to squamate reptiles have been isolated from the genomes of lacertid lizards and sequenced. These retroposons, which we called Squam1, are 360–390 bp long and contain a region similar to the tRNA gene sequence at the 5’ end. This family has also been detected in representatives of other reptile families (varanids, iguanids (Anolis), gekkonids, and snakes), being absent from the genomes of crocodiles as well as amphibians, birds, and mammals. The primary structures of Squam1 copies have been comprehensively analyzed and compared with GenBank sequences. The genomes of most taxa contain two to three SINE subfamilies with specific diagnostic features in their primary structures. Individual similarity between the copies within each taxon is about 85%, with intrageneric similarity being only slightly higher. A comparison of consensus sequences between different lizard families has shown that Squam1 may be a convenient phylogenetic marker for this group of reptiles, having a number of both apomorphic and more or less pronounced synapomorphic features. By this criterion, snakes slightly differ from lizards but obviously belong to the same clade. However, they show no special affinity to varanids as the putative closest relatives of snakes, compared to other lizards.     

有瓣蝇类分类、系统发育及演化

有瓣蝇类(Calyptratae)隶属于昆虫纲(Insecta)四大超适应辐射类群之一的双翅目(Diptera),占双翅目已知物种多样性的近20%。有瓣蝇类分布广泛,生物学习性极为多样,在维系生态系统稳定中发挥着重要作用,是媒介、法医、传粉和天敌昆虫学研究领域的热点类群,也是探究双翅目系统演化及其成功适应辐射的关键类群。为了还原有瓣蝇类的演化历史,许多著名昆虫学者先后对该类昆虫开展过不同层面的研究。有瓣蝇类的单系性得到了普遍支持,并被分为3个总科——虱蝇总科(Hippoboscoidea)、蝇总科(Muscoidea)和狂蝇总科(Oestroidea),其中单系的狂蝇总科与多系的蝇总科聚为一支,再与虱蝇总科成为姐妹群。在科级阶元水平,蝠蝇科(Streblidae)(虱蝇总科)、花蝇科(Anthomyiidae)(蝇总科)、丽蝇科(Calliphoridae)(狂蝇总科)、邻寄蝇科(Rhinophoridae)(狂蝇总科)等类群的单系性仍有待验证,且新的科仍在不断被建立［如粉蝇科(Polleniidae)、乌鲁鲁蝇科(Ulurumyiidae)］,因此,有瓣蝇类科级系统发育关系仍不十分明晰。已有研究对虱蝇总科虱蝇科(Hippoboscidae)、蝠蝇科、蛛蝇科(Nycteribiidae),蝇总科蝇科(Muscidae)、粪蝇科(Scathophagidae),狂蝇总科麻蝇科(Sarcophagidae)、狂蝇科(Oestridae)胃蝇亚科(Gasterophilinae)的演化历史进行研究,明确了起源与扩散、寄主转移、取食策略等关键生物学习性的演化历史。但由于部分关键类群生活史信息的缺失,以及尚未有效解决的系统发育关系,有瓣蝇类演化历史仍有许多待解之谜。本文综述了有瓣蝇类分类、系统发育及演化研究进展,是在系统学研究进入系统发育基因组学时代后对该类群相关研究进展的首次全面总结。     

Functional and evolutionary morphology of lingual feeding in squamate reptiles: phylogenetics and kinematics

Use of the tongue as a prehensile organ during the ingestion stage of feeding in lizards was studied cinegraphically in seven species. Within Squamata, lingual prehension is limited to a single clade, the Iguania (Iguanidae, Agamidae and Chamaeleontidae), which includes all 'fleshy-tongued' lizards. All remaining squamates (Scleroglossa) use the jaws alone for prey prehension. Lingual prehension and a 'fleshy' tongue are primitive squamate characteristics. Kinematically, lingual ingestion cycles are similar to previously described transport cycles in having slow open, fast open, fast close and slow close-power stroke phases. Tongue movements are sequentially correlated with jaw movements as they are in transport. However, during ingestion, anterior movement of the tongue includes an extra-oral, as well as intra-oral component. Tongue protrusion results in a pronounced slow open-II phase at a large gape distance. A high degree of variability in quantitative aspects of ingestion and transport cycles suggests that modulation through sensory feedback is an important aspect of lizard feeding. Preliminary evidence indicates an important role for hyoid movement in tongue protrusion. Our results are consistent with the Bramble & Wake (1985) model generalized feeding cycle and support their contention that specialized feeding mechanisms often represent modifications of a basic pattern, particularly modification of the slow open phase.