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.     

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.     

The phylogenetic placement of Psechridae within Entelegynae and the convergent origin of orb‐like spider webs

Evolutionary convergence of phenotypic traits provides evidence for their functional success. The origin of the orb web was a critical event in the diversification of spiders that facilitated a spectacular radiation of approximately 12 000 species and promoted the evolution of novel web types. How the orb web evolved from ancestral web types, and how many times orb‐like architectures evolved in spiders, has been debated for a long time. The little known spider genus Fecenia (Psechridae) constructs a web that resembles the archetypical orb web, but morphological data suggest that Psechridae (Psechrus + Fecenia) does not belong in Orbiculariae, the ‘true orb weavers’, but to the ‘retrolateral tibial apophysis (RTA) clade’ consisting mostly of wandering spiders, but also including spiders building less regular webs. Yet, the data are sparse and no molecular phylogenetic study has estimated Fecenia's exact position in the tree of life. Adding new data to sequences pulled from GenBank, we reconstruct a phylogeny of Entelegynae and phylogenetically test the monophyly and placement of Psechridae, and in doing so, the alternative hypotheses of monophyletic origin of the orb web and the pseudo‐orb versus their independent origins, a potentially spectacular case of behavioural convergence. We also discuss the implications of our results for Entelegynae systematics. Our results firmly place a monophyletic Psechridae within the RTA clade, phylogenetically distant from true orb weavers. The architectural similarities of the orb and the pseudo‐orb are therefore clearly convergent, as also suggested by detailed comparisons of these two web types, as well as the spiders' web‐building behaviours and ontogenetic development. The convergence of Fecenia webs with true orbs provides a remarkable opportunity to investigate how these complex sets of traits may have interacted during the evolution of the orb.     

The origin of multiplacophorans – convergent evolution in Aculiferan molluscs

Abstract: Multiplacophorans are Palaeozoic (Silurian to Permian) stem group polyplacophorans with 17 shell plates in a particular arrangement of single terminal plates separated by three columns of plates forming five transverse rows. Their distinctive morphology has prompted disparate interpretations of their relationship to polyplacophorans. Some features are strikingly similar to crown group polyplacophorans and even to some living families. Here we describe two Devonian forms, Protobalanus spinicoronatus sp. nov., a hercolepadid from northeast Ohio, USA, and Hannestheronia australis gen. et sp. nov., a strobilepid from South Africa. Using the results from a Bayesian relaxed molecular clock to test competing scenarios of the relationship of multiplacophorans to crown group polyplacophorans, we demonstrate that multiplacophorans are stem group polyplacophorans in which certain characters of the crown group evolved convergently.     

Evidence for convergent evolution of a neocortex‐like structure in a late Permian therapsid

The special sensory, motor, and cognitive capabilities of mammals mainly depend upon the neocortex, which is the six‐layered cover of the mammalian forebrain. The origin of the neocortex is still controversial and the current view is that larger brains with neocortex first evolved in late Triassic Mammaliaformes. Here, we report the earliest evidence of a structure analogous to the mammalian neocortex in a forerunner of mammals, the fossorial anomodont Kawingasaurus fossilis from the late Permian of Tanzania. The endocranial cavity of Kawingasaurus is almost completely ossified, which allowed a less hypothetical virtual reconstruction of the brain endocast to be generated. A parietal foramen is absent. A small pit between the cerebral hemispheres is interpreted as a pineal body. The inflated cerebral hemispheres are demarcated from each other by a median sulcus and by a possible rhinal fissure from the rest of the endocast. The encephalization quotient estimated by using the method of Eisenberg is 0.52, which is 2–3 times larger than in other nonmammalian synapsids. Another remarkable feature are the extremely ramified infraorbital canals in the snout. The shape of the brain endocast, the extremely ramified maxillary canals as well as the small frontally placed eyes suggest that special sensory adaptations to the subterranean habitat such as a well developed sense of touch and binocular vision may have driven the parallel evolution of an equivalent of the mammalian neocortex and a mammal‐like lemnothalamic visual system in Kawingasaurus . The gross anatomy of the brain endocast of Kawingasaurus supports the Outgroup Hypothesis, according to which the neocortex evolved from the dorsal pallium of an amphibian‐like ancestor, which receives sensory projections from the lemnothalamic pathway. The enlarged brain as well as the absence of a parietal foramen may be an indication for a higher metabolic rate of Kawingasaurus compared to other nonmammalian synapsids.     

Divergent in shape and convergent in function: Adaptive evolution of the mandible in Sub‐Antarctic mice

Convergent evolution in similar environments constitutes strong evidence of adaptive evolution. Transported with people around the world, house mice colonized even remote areas, such as Sub‐Antarctic islands. There, they returned to a feral way of life, shifting towards a diet enriched in terrestrial macroinvertebrates. Here, we test the hypothesis that this triggered convergent evolution of the mandible, a morphological character involved in food consumption. Mandible shape from four Sub‐Antarctic islands was compared to phylogeny, tracing the history of colonization, and climatic conditions. Mandible shape was primarily influenced by phylogenetic history, thus discarding the hypothesis of convergent evolution. The biomechanical properties of the jaw were then investigated. Incisor in‐lever and temporalis out‐lever suggested an increase in the velocity of incisor biting, in agreement with observations on various carnivorous and insectivorous rodents. The mechanical advantage related to incisor biting also revealed an increased functional performance in Sub‐Antarctic populations, and appears to be an adaptation to catch prey more efficiently. The amount of change involved was larger than expected for a plastic response, suggesting microevolutionary processes were evolved. This study thus denotes some degree of adaptive convergent evolution related to changes in habitat‐related changes in dietary items in Sub‐Antarctic mice, but only regarding simple, functionally relevant aspects of mandible morphology.     

The evolution of bat nucleic acid‐sensing Toll‐like receptors

We characterized the nucleic acid‐sensing Toll‐like receptors (TLR) of a New World bat species, the common vampire bat (Desmodus rotundus), and through a comparative molecular evolutionary approach searched for general adaptation patterns among the nucleic acid‐sensing TLRs of eight different bats species belonging to three families (Pteropodidae, Vespertilionidae and Phyllostomidae). We found that the bat TLRs are evolving slowly and mostly under purifying selection and that the divergence pattern of such receptors is overall congruent with the species tree, consistent with the evolution of many other mammalian nuclear genes. However, the chiropteran TLRs exhibited unique mutations fixed in ligand‐binding sites, some of which involved nonconservative amino acid changes and/or targets of positive selection. Such changes could potentially modify protein function and ligand‐binding properties, as some changes were predicted to alter nucleic acid binding motifs in TLR 9. Moreover, evidence for episodic diversifying selection acting specifically upon the bat lineage and sublineages was detected. Thus, the long‐term adaptation of chiropterans to a wide variety of environments and ecological niches with different pathogen profiles is likely to have shaped the evolution of the bat TLRs in an order‐specific manner. The observed evolutionary patterns provide evidence for potential functional differences between bat and other mammalian TLRs in terms of resistance to specific pathogens or recognition of nucleic acids in general.     

The effect of sex on the repeatability of evolution in different environments

The adaptive function of sex has been extensively studied, while less consideration has been given to the potential downstream consequences of sex on evolution. Here, we investigate one such potential consequence, the effect of sex on the repeatability of evolution. By affecting the repeatability of evolution, sex could have important implications for biodiversity, and for our ability to make predictions about the outcome of environmental change. We allowed asexual and sexual populations of Chlamydomonas reinhardtii to evolve in novel environments and monitored both their change in fitness and variance in fitness after evolution. Sex affected the repeatability of evolution by changing the importance of the effect of selection, chance, and ancestral constraints on the outcome of the evolutionary process. In particular, the effects of sex were highly dependent on the initial genetic composition of the population and on the environment. Given the lack of a consistent effect of sex on repeatability across the environments used here, further studies to dissect in more detail the underlying reasons for these differences as well as studies in additional environments are required if we are to have a general understanding of the effects of sex on the repeatability of evolution.     

Evolution of reproductive isolation as a by‐product of divergent life‐history evolution in laboratory populations of Drosophila melanogaster

We show that two complementary asymmetric isolating mechanisms, likely mediated by divergence in body size, underlie the evolution of incipient reproductive isolation between a set of Drosophila melanogaster populations selected for rapid development and their ancestral controls. Selection has led to great reduction in body size in the fast developing lines. Small males belonging to fast developing lines obtain few matings with large control females, both in presence and absence of large control line males, giving rise to unidirectional, premating isolation caused by sexual selection. Conversely, small selected line females suffer greatly increased mortality following mating with large control males, causing unidirectional postcopulatory prezygotic isolation. We discuss preliminary evidence for evolution of reduced male harm caused to females upon mating in the fast developing lines, and speculate that the females from these lines have coevolved reduced resistance to male harm such that they can no longer resist the harm caused by males from control lines. This potentially implicates differing levels of sexual conflict in creating reproductive barrier between the selected line females and the control males. We also show that a large difference in development time is not sufficient to cause postzygotic incompatibilities in the two sets of populations reaffirming the belief that prezygotic isolation can evolve much earlier than postzygotic isolation.     

Rates and patterns in the evolution of snake-like body form in squamate reptiles: evidence for repeated re-evolution of lost digits and long-term persistence of intermediate body forms

An important challenge in evolutionary biology is to understand how major changes in body form arise. The dramatic transition from a lizard-like to snake-like body form in squamate reptiles offers an exciting system for such research because this change is replicated dozens of times. Here, we use morphometric data for 258 species and a time-calibrated phylogeny to explore rates and patterns of body-form evolution across squamates. We also demonstrate how time-calibrated phylogenies may be used to make inferences about the time frame over which major morphological transitions occur. Using the morphometric data, we find that the transition from lizard-like to snake-like body form involves concerted evolution of limb reduction, digit loss, and body elongation. These correlations are similar across squamate clades, despite very different ecologies and >180 million years (My) of divergence. Using the time-calibrated phylogeny and ancestral reconstructions, we find that the dramatic transition between these body forms can occur in 20 My or less, but that seemingly intermediate morphologies can also persist for tens of millions of years. Finally, although loss of digits is common, we find statistically significant support for at least six examples of the re-evolution of lost digits in the forelimb and hind limb.     

Parallel evolution of site‐specific changes in divergent caribou lineages

The parallel evolution of phenotypes or traits within or between species provides important insight into the basic mechanisms of evolution. Genetic and genomic advances have allowed investigations into the genetic underpinnings of parallel evolution and the independent evolution of similar traits in sympatric species. Parallel evolution may best be exemplified among species where multiple genetic lineages, descended from a common ancestor, colonized analogous environmental niches, and converged on a genotypic or phenotypic trait. Modern North American caribou (Rangifer tarandus) originated from three ancestral sources separated during the Last Glacial Maximum (LGM): the Beringian–Eurasian lineage (BEL), the North American lineage (NAL), and the High Arctic lineage (HAL). Historical introgression between the NAL and the BEL has been found throughout Ontario and eastern Manitoba. In this study, we first characterized the functional differentiation in the cytochrome‐b (cytB) gene by identifying nonsynonymous changes. Second, the caribou lineages were used as a direct means to assess site‐specific parallel changes among lineages. There was greater functional diversity within the NAL despite the BEL having greater neutral diversity. The patterns of amino acid substitutions occurring within different lineages supported the parallel evolution of cytB amino acid substitutions suggesting different selective pressures among lineages. This study highlights the independent evolution of identical amino acid substitutions within a wide‐ranging mammal species that have diversified from different ancestral haplogroups and where ecological niches can invoke parallel evolution.     

The evolutionary characteristics and structural biology of Gallus toll‐like receptor 21

Toll‐like receptors (TLRs) are an important part of the innate immune system, acting as a first line of defense against many invading pathogens. The ligand known to bind Gallus toll‐like receptor 21 (gTLR21) is the unmethylated cytosine phosphate guanine dideoxy nucleotide motif; however, the evolutionary characteristics and structural biology of gTLR21 are poorly elaborated. Our results suggest that gTLR21 is phylogenetically and evolutionarily related to the TLR11 family and is perhaps a close ortholog of the Mus TLR13. Structural biology of homology modeling of the gTLR21 ectodomain structure suggests that it has no Z‐loop like that seen in Mus TLR9. The cytosolic toll‐IL‐1 receptor region of gTLR21 contains a central 4‐stranded parallel β‐sheet (βA‐βD) surrounded by 5 α‐helices (αA‐αE) on both sides, a highly conserved structure also seen in other TLRs. Molecular docking analysis reveals that the gTLR21 ectodomain has the potential to distinguish between different ligands. Homodimer analysis results also suggest that Phe842 and Pro844 of the BB loop and Cys876 of the αC helix in gTLR21 are conserved in other cytosolic toll‐IL‐1 receptor domains of other TLRs and may contribute to the docking of homodimers. Our study on the evolutionary characteristics and structural biology of gTLR21 reveals that the molecule may have a broader role to play in innate immune system; however, further experimental validation is required to confirm our findings.     

Seasonal environments drive convergent evolution of a faster pace‐of‐life in tropical butterflies

New ecological niches that may arise due to climate change can trigger diversification, but their colonisation often requires adaptations in a suite of life‐history traits. We test this hypothesis in species‐rich Mycalesina butterflies that have undergone parallel radiations in Africa, Asia, and Madagascar. First, our ancestral state reconstruction of habitat preference, using c. 85% of extant species, revealed that early forest‐linked lineages began to invade seasonal savannahs during the late Miocene‐Pliocene. Second, rearing replicate pairs of forest and savannah species from the African and Malagasy radiation in a common garden experiment, and utilising published data from the Asian radiation, demonstrated that savannah species consistently develop faster, have smaller bodies, higher fecundity with an earlier investment in reproduction, and reduced longevity, compared to forest species across all three radiations. We argue that time‐constraints for reproduction favoured the evolution of a faster pace‐of‐life in savannah species that facilitated their persistence in seasonal habitats.     

The evolution of alternative mechanisms that promote outcrossing in Annonaceae,a self‐compatible family of early‐divergent angiosperms

Annonaceae flowers are generally hermaphroditic and show high levels of outcrossing, but unlike many other early‐divergent angiosperms lack a self‐incompatibility mechanism. We reassess the diversity of mechanisms that have evolved to avoid self‐pollination in the family. Protogyny occurs in all hermaphroditic flowers in the family, preventing autogamy but not geitonogamy. Herkogamy is rare in Annonaceae and is likely to be less effective as beetles move randomly around the flowers in search of food and/or mates. Geitonogamy is largely avoided in Annonaceae by combining protogyny with floral synchrony, manifested as either pistillate/staminate‐phase synchrony (in which pistillate‐phase and staminate‐phase flowers do not co‐occur on an individual) or heterodichogamy (in which two phenologically distinct and reproductively isolated morphs coexist in populations). Unisexual flowers have evolved independently in several lineages, mostly as andromonoecy (possibly androdioecy). Functionally monoecious populations have evolved from andromonoecious ancestors through the loss of staminate function in structurally hermaphroditic flowers. This has been achieved in different ways, including incomplete pollen/stamen development and delayed anther dehiscence. Angiosperms display an enormous diversity of mechanisms to promote xenogamy, many of which are easily overlooked without fieldwork. Floral phenology is particularly important, especially cryptic differences in timing of organ maturation or abscission. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 174 , 93–109.