Despite the prevalence of sexual reproduction across eukaryotes, there is a remarkable diversity of sex‐determination mechanisms. The underlying causes of this diversity remain unclear, and it is ...unknown whether there are convergent trends in the directionality of turnover in sex‐determination mechanisms. We used the recently assembled Tree of Sex database to assess patterns in the evolution of sex‐determination systems in the remarkably diverse vertebrate clades of teleost fish, squamate reptiles and amphibians. Contrary to theoretical predictions, we find no evidence that the evolution of separate sexes is irreversible, as transitions from separate sexes to hermaphroditism occur at higher rates than the reverse in fish. We also find that transitions from environmental sex determination to genetic sex determination occur at higher rates than the reverse in both squamates and fish, suggesting that genetic sex determination is more stable. However, our data are not consistent with the hypothesis that heteromorphic sex chromosomes are an “evolutionary trap.” Rather, we find similar transition rates between homomorphic and heteromorphic sex chromosomes in both fish and amphibians, and to environmental sex determination from heteromorphic vs. homomorphic sex chromosome systems in fish. Finally, we find that transitions between male and female heterogamety occur at similar rates in amphibians and squamates, while transitions to male heterogamety occur at higher rates in fish. Together, these results provide the most comprehensive view to date of the evolution of vertebrate sex determination in a phylogenetic context, providing new insight into long‐standing questions about the evolution of sexual reproduction.
•Brain allometry across higher macroevolutionary hierarchies in snakes seems conserved.•In lizards the macroevolutionary brain allometry at higher hierarchies is variable.•Brain size in Crotalinae ...pit-vipers evolved without anatomical energetic trade-offs.•Body design could drive conservation of macroevolutionary brain allometry in snakes.
Despite historical interest in brain size evolution in vertebrates, few studies have assessed variation in brain size in squamate reptiles such as snakes and lizards. Here, we analyzed the pattern of brain allometry at macroevolutionary scale in snakes and lizards, using body mass and snout vent length as measures of body size. We also assessed potential energetic trade-offs associated with relative brain size changes in Crotalinae vipers. Body mass showed a conserved pattern of brain allometry across taxa of snakes, but not in lizards. Body length favored changes of brain allometry in both snakes and lizards, but less variability was observed in snakes. Moreover, we did not find evidence for trade-offs between brain size and the size of other organs in Crotalinae. Thus, despite the contribution of body elongation to changes in relative brain size in squamate reptiles, snakes present low variation in brain allometry across taxa. Although the mechanisms driving this conserved pattern are unknown, we hypothesize that the snake body plan plays an important role in balancing the energetic demands of brain and body size increase at macroevolutionary scales. We encourage future research on the evolution of brain and body size in snakes to test this hypothesis.
Loss of limbs evolved many times in squamate reptiles. Here we investigated the genomic basis of convergent limb loss in reptiles. We sequenced the genomes of a closely related pair of ...limbless-limbed gymnophthalmid lizards and performed a comparative genomic analysis including five snakes and the limbless glass lizard. Our analysis of these three independent limbless lineages revealed that signatures of shared sequence or transcription factor binding site divergence in individual limb regulatory elements are generally rare. Instead, shared divergence occurs more often at the level of signaling pathways, involving different regulatory elements associated with the same limb genes (such as Hand2 or Hox) and/or patterning mechanisms (such as Shh signaling). Interestingly, although snakes are known to have mutations in the Shh ZRS limb enhancer, this enhancer lacks relevant mutations in limbless lizards. Thus, different mechanisms could contribute to limb loss, and there are likely multiple evolutionary paths to limblessness in reptiles.
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•Limb enhancer divergence is more pronounced in snakes than in limbless lizards•Divergence in individual limb regulatory elements is largely lineage specific•Shared divergence signatures involve the same limb genes or patterning mechanisms•The Shh-regulating ZRS limb enhancer lacks relevant mutations in limbless lizards
Limb reduction or loss in reptiles has evolved repeatedly. Investigating the genomic basis of convergent losses of limbs in three reptile lineages, Roscito et al. show that signatures of molecular convergence are generally rare. This suggests that there are multiple mechanisms and evolutionary paths leading to limblessness.
Aim: To investigate the historical distribution of the Cerrado across Quaternary climatic fluctuations and to generate historical stability maps to test: (1) whether the 'historical climate' ...stability hypothesis explains squamate reptile richness in the Cerrado; and (2) the hypothesis of Pleistocene connections between savannas located north and south of Amazonia. Location: The Cerrado, a savanna biome and a global biodiversity hotspot distributed mainly in central Brazil. Methods: We generated occurrence datasets from 1000 presence points randomly selected from the entire distribution of the Cerrado, as determined by two spatial definitions. We modelled the potential Cerrado distribution by implementing a maximum-entropy machine-learning algorithm across four time projections: current, mid-Holocene (6 ka), Last Glacial Maximum (LGM, 21 ka) and Last Interglacial (LIG, 120 ka). We generated historical stability maps (refugiai areas) by overlapping presence/absence projections of all scenarios, and checked consistencies with qualitative comparisons with available fossil pollen records. We built a spatially explicit simultaneous autoregressive model to explore the relationship between current climate, climatic stability, and squamate species richness. Results: Models predicted the LGM and LIG as the periods of narrowest and widest Cerrado distributions, respectively, and were largely corroborated by palynological evidence. We found evidence for two savanna corridors (eastern coastal during the LIG, and Andean during the LGM) and predicted a large refugiai area in the north-eastern Cerrado (Serra Geral de Goiás refugium). Variables related to climatic stability predicted squamate richness better than present climatic variables did. Main conclusions: Our results indicate that Bolivian savannas should be included within the Cerrado range and that the Cerrado's biogeographical counterparts are not Chaco and Caatinga but rather the disjunct savannas of the Guyana shield plateaus. Climatic stability is a good predictor of Cerrado squamate richness, and our stability maps could be used in future studies to test diversity patterns and genetic signatures of different taxonomic groups and as a higher-order landscape biodiversity surrogate for conservation planning.
Fangs are a putative key innovation that revolutionized prey capture and feeding in snakes, and - along with their associated venom phenotypes - have made snakes perhaps the most ...medically-significant vertebrate animals. Three snake clades are known for their forward-positioned fangs, and these clades (Elapidae, Viperidae, and Atractaspidinae) contain the majority of snakes that are traditionally considered venomous. However, many other snakes are "rear-fanged": they possess potentially venom-delivering teeth situated at the rear end of the upper jaw. Quantification of fang phenotypes - and especially those of rear-fanged species - has proved challenging or impossible owing to the small size and relative rarity of many such snakes. Consequently, it has been difficult to understand the evolutionary history of both venom and prey-capture strategies across extant snakes. We quantified variation in the dentition of 145 colubriform ("advanced") snake species using microCT scanning and compared dental characters with ecological data on species' diet and prey capture method(s) to understand broader patterns in snake fang evolution. Dental traits such as maxilla length, tooth number, and fang size show strong phylogenetic signal across Colubriformes. We find extreme heterogeneity and evolutionary lability in the rear-fanged phenotype in colubrid (colubrine, dipsadine, and natricine lineages) and lamprophiid snakes, in contrast to relative uniformity in the front fanged phenotypes of other groups (vipers and, to a lesser extent, elapids). Fang size and position are correlated with venom-use in vipers, elapids, and colubrid snakes, with the latter group shifting fangs anteriorly by shortening the entire maxillary bone. We find that maxilla length and tooth number may also be correlated with the evolution of dietary specialization. Finally, an ancestral state reconstruction suggests that fang loss is a recurring phenomenon in colubrid snakes, likely accompanied by shifts in diet and prey capture mode. Our study provides a framework for quantifying the complex morphologies associated with venom use in snakes. Our results suggest that fang phenotypes, and particularly the rear-fanged phenotype, in snakes are both diverse and labile, facilitating a wide range of ecological strategies and contributing to spectacular radiations of these organisms in tropical and subtropical biomes worldwide.
Lepidosauria (lizards, snakes, tuatara) is a globally distributed and ecologically important group of over 9,000 reptile species. The earliest fossil records are currently restricted to the Late ...Triassic and often dated to 227 million years ago (Mya). As these early records include taxa that are relatively derived in their morphology (e.g. Brachyrhinodon), an earlier unknown history of Lepidosauria is implied. However, molecular age estimates for Lepidosauria have been problematic; dates for the most recent common ancestor of all lepidosaurs range between approximately 226 and 289 Mya whereas estimates for crown-group Squamata (lizards and snakes) vary more dramatically: 179 to 294 Mya. This uncertainty restricts inferences regarding the patterns of diversification and evolution of Lepidosauria as a whole.
Here we report on a rhynchocephalian fossil from the Middle Triassic of Germany (Vellberg) that represents the oldest known record of a lepidosaur from anywhere in the world. Reliably dated to 238-240 Mya, this material is about 12 million years older than previously known lepidosaur records and is older than some but not all molecular clock estimates for the origin of lepidosaurs. Using RAG1 sequence data from 76 extant taxa and the new fossil specimens two of several calibrations, we estimate that the most recent common ancestor of Lepidosauria lived at least 242 Mya (238-249.5), and crown-group Squamata originated around 193 Mya (176-213).
A Early/Middle Triassic date for the origin of Lepidosauria disagrees with previous estimates deep within the Permian and suggests the group evolved as part of the faunal recovery after the end-Permain mass extinction as the climate became more humid. Our origin time for crown-group Squamata coincides with shifts towards warmer climates and dramatic changes in fauna and flora. Most major subclades within Squamata originated in the Cretaceous postdating major continental fragmentation. The Vellberg fossil locality is expected to become an important resource for providing a more balanced picture of the Triassic and for bridging gaps in the fossil record of several other major vertebrate groups.
It is of fundamental importance for the field of evolutionary biology to understand when and why major evolutionary transitions occur. Live‐bearing young (viviparity) is a major evolutionary change ...and has evolved from egg‐laying (oviparity) independently in many vertebrate lineages and most abundantly in lizards and snakes. Although contemporary viviparous squamate species generally occupy cold climatic regions across the globe, it is not known whether viviparity evolved as a response to cold climate in the first place. Here, we used available published time‐calibrated squamate phylogenies and parity data on 3,498 taxa. We compared the accumulation of transitions from oviparity to viviparity relative to background diversification and a simulated binary trait. Extracting the date of each transition in the phylogenies and informed by 65 my of global palaeoclimatic data, we tested the nonexclusive hypotheses that viviparity evolved under the following: (a) cold, (b) long‐term stable climatic conditions and (c) with background diversification rate. We show that stable and long‐lasting cold climatic conditions are correlated with transitions to viviparity across squamates. This correlation of parity mode and palaeoclimate is mirrored by background diversification in squamates, and simulations of a binary trait also showed a similar association with palaeoclimate, meaning that trait evolution cannot be separated from squamate lineage diversification. We suggest that parity mode transitions depend on environmental and intrinsic effects and that background diversification rate may be a factor in trait diversification more generally.
Frequency of transitions from oviparity to viviparity and palaeoclimate. (a) Empirically estimated transitions from oviparity to viviparity in squamates (dark grey) and the ratio of oxygen isotope (δ18O) as proxy for global mean temperature (light grey) are displayed per million years from 65 million years ago to present. Temperature (y‐axis) and number of transitions (z‐axis) are shown as smoothed lines (spanλ = 0.25).
Understanding the mechanisms by which the abiotic and biotic requirements of species, or ecological niches, change over time is a central issue in evolutionary biology. Niche evolution is poorly ...understood at both the macroecological and macroevolutionary scales, as niches can shift over short periods of time but appear to change more slowly over longer timescales. Although reconstructing past niches has always been a major concern for palaeontologists and evolutionary biologists, only a few recent studies have successfully determined the factors that affect niche evolution. Here, we compare the evolution of climatic niches in four main groups of terrestrial vertebrates using a modelling approach integrating both palaeontological and neontological data, and large-scale datasets that contain information on the current distributions, phylogenetic relationships and fossil records for a total of 11,465 species. By reconstructing historical shifts in geographical ranges and climatic niches, we show that niche shifts are significantly faster in endotherms (birds and mammals) than in ectotherms (squamates and amphibians). We further demonstrate that the diversity patterns of the four clades are directly affected by the rate of niche evolution, with fewer latitudinal shifts in ectotherms.
The identification of conserved loci across genomes, along with advances in target capture methods and high‐throughput sequencing, has helped spur a phylogenomics revolution by enabling researchers ...to gather large numbers of homologous loci across clades of interest with minimal upfront investment in locus design. Target capture for vertebrate animals is currently dominated by two approaches—anchored hybrid enrichment (AHE) and ultraconserved elements (UCE)—and both approaches have proven useful for addressing questions in phylogenomics, phylogeography and population genomics. However, these two sets of loci have minimal overlap with each other; moreover, they do not include many traditional loci that that have been used for phylogenetics. Here, we combine across UCE, AHE and traditional phylogenetic gene locus sets to generate the Squamate Conserved Loci set, a single integrated probe set that can generate high‐quality and highly complete data across all three loci types. We use these probes to generate data for 44 phylogenetically disparate taxa that collectively span approximately 33% of terrestrial vertebrate diversity. Our results generated an average of 4.29 Mb across 4709 loci per individual, of which an average of 2.99 Mb was sequenced to high enough coverage (≥10×) to use for population genetic analyses. We validate the utility of these loci for both phylogenomic and population genomic questions, provide a comparison among these locus sets of their relative usefulness and suggest areas for future improvement.
Evolutionary transitions in life‐history strategies, such as the shift from egg‐laying to live birth (viviparity) are of great interest to evolutionary biologists. In squamate reptiles, several ...hypotheses have been proposed to explain viviparity including the cold climate hypothesis, maternal manipulation hypothesis, hypoxia hypothesis, and several others. We used two approaches: first we studied 45 species of Liolaemus, a genus where nearly 50% of species are viviparous, using a diverse ecophysiological dataset to examine the cold climate and maternal manipulation hypotheses. We collected environmental thermal data (accounting for elevational differences among species), physiological traits including preferred body temperature and its coefficient of variation as an indicator of precision in thermoregulation. Additionally, we collected standard metabolic rates for 23 of the 45 species. In one clade (the darwinii group of species) with both reproductive modes, we ran our second approach. We tested for differences in thermal physiology and metabolic rates between viviparous and oviparous species during pregnancy and non‐pregnancy periods. The cold climate hypothesis received strong support because viviparous species occur in sites with colder air temperatures (including areas at both higher elevations and latitudes) compared with oviparous species. Our detailed analysis showed that the maternal manipulation hypothesis also is supported; pregnant viviparous females show lower variation in their selected temperature. Our evidence suggests that the Andean orogeny is likely to have played a key role in the diversification of Liolaemus lizards and the evolution of viviparity in this clade may have been driven by a variety of physiological advantages accrued at different stages of embryogenesis and over evolutionary time. Thus, historical climate changes may have led to egg retention and may have been accompanied by other adaptations such as thermoregulation precision.
Several hypotheses have been proposed to explain viviparity in Reptiles including the cold climate hypothesis, maternal manipulation hypothesis, hypoxia hypothesis, and several others. We collected environmental thermal data, preferred body temperature, its coefficient of variation (as an indicator of precision in thermoregulation) and standard metabolic rates for several species of Liolaemus. We tested for differences in thermal physiology and metabolic rates between viviparous and oviparous species during pregnancy and non‐pregnancy periods. Both, the cold climate and the maternal manipulation hypotheses were supported. Viviparous species occur in sites with colder air temperatures and pregnant viviparous females show lower variation in their selected temperature than oviparous gravid females. Historical climate changes may have led to egg retention and may have been accompanied by other adaptations such as thermoregulation precision.
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