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Adhesive toe pads have evolved numerous times over lizard evolutionary history, most notably in geckos. Despite significant variation in adult toe pad morphology across independent origins of toe pads, early developmental patterns of toe pad morphogenesis are similar among distantly related species. In these distant phylogenetic comparisons, toe pad variation is achieved during the later stages of development. We aimed to understand how toe pad variation is generated among species sharing a single evolutionary origin of toe pads (house geckos—Hemidactylus). We investigated toe pad functional variation and developmental patterns in three species of Hemidactylus, ranging from highly scansorial (H. platyurus), to less scansorial (H. turcicus), to fully terrestrial (H. imbricatus). We found that H. platyurus generated significantly greater frictional adhesive force and exhibited much larger toe pad area relative to the other two species. Furthermore, differences in the offset of toe pad extension phase during embryonic development results in the variable morphologies seen in adults. Taken together, we demonstrate how morphological variation is generated in a complex structure during development and how that variation relates in important functional outcomes.

 

Library preparation protocols for most sequencing technologies involve PCR amplification of the template DNA, which open the possibility that a given template DNA molecule is sequenced multiple times. Reads arising from this phenomenon, known as PCR duplicates, inflate the cost of sequencing and can jeopardize the reliability of affected experiments. Despite the pervasiveness of this artefact, our understanding of its causes and of its impact on downstream statistical analyses remains essentially empirical. Here, we develop a general quantitative model of amplification distortions in sequencing data sets, which we leverage to investigate the factors controlling the occurrence of PCR duplicates. We show that the PCR duplicate rate is determined primarily by the ratio between library complexity and sequencing depth, and that amplification noise (including in its dependence on the number of PCR cycles) only plays a secondary role for this artefact. We confirm our predictions using new and published RAD‐seq libraries and provide a method to estimate library complexity and amplification noise in any data set containing PCR duplicates. We discuss how amplification‐related artefacts impact downstream analyses, and in particular genotyping accuracy. The proposed framework unites the numerous observations made on PCR duplicates and will be useful to experimenters of all sequencing technologies where DNA availability is a concern.

 

Abstract How developmental modifications produce key innovations, which subsequently allow for rapid diversification of a clade into new adaptive zones, has received much attention. However, few studies have used a robust comparative framework to investigate the influence of evolutionary and developmental constraints on the origin of key innovations, such as the adhesive toe pad of lizards. Adhesive toe pads evolved independently at least 16 times in lizards, allowing us to examine whether the patterns observed are general evolutionary phenomena or unique, lineage-specific events. We performed a high-resolution comparison of plantar scale development in 14 lizard species in Anolis and geckos, encompassing five independent origins of toe pads (one in Anolis, four in geckos). Despite substantial evolutionary divergence between Anolis and geckos, we find that these clades have undergone similar developmental modifications to generate their adhesive toe pads. Relative to the ancestral plantar scale development, in which scale ridges form synchronously along the digit, both padded geckos and Anolis exhibit scansor formation in a distal-to-proximal direction. Both clades have undergone developmental repatterning and, following their origin, modifications in toe pad morphology occurred through relatively minor developmental modifications, suggesting that developmental constraints governed the diversification of the adhesive toe pad in lizards. 

Among the most specialized integumentary outgrowths in amniotes are the adhesive, scale-like scansors and lamellae on the digits of anoles and geckos. Less well-known are adhesive tail pads exhibited by 21 gecko genera. While described over 120 years ago, no studies have quantified their possible adhesive function or described their embryonic development. Here, we characterize adult and embryonic morphology and adhesive performance of crested gecko ( Correlophus ciliatus ) tail pads. Additionally, we use embryonic data to test whether tail pads are serial homologues to toe pads. External morphology and histology of C . ciliatus tail pads are largely similar to tail pads of closely related geckos. Functionally, C . ciliatus tail pads exhibit impressive adhesive ability, hypothetically capable of holding up to five times their own mass. Tail pads develop at approximately the same time during embryogenesis as toe pads. Further, tail pads exhibit similar developmental patterns to toe pads, which are markedly different from non-adhesive gecko toes and tails. Our data provide support for the serial homology of adhesive tail pads with toe pads. 

Loss and reduction in paired appendages are common in vertebrate evolution. How often does such convergent evolution depend on similar developmental and genetic pathways? For example, many populations of the threespine stickleback and ninespine stickleback (Gasterosteidae) have independently evolved pelvic reduction, usually based on independent mutations that caused reducedPitx1expression. ReducedPitx1expression has also been implicated in pelvic reduction in manatees. Thus, hindlimb reduction stemming from reducedPitx1expression has arisen independently in groups that diverged tens to hundreds of millions of years ago, suggesting a potential for repeated use ofPitx1across vertebrates. Notably, hindlimb reduction based on the reduction inPitx1expression produces left‐larger directional asymmetry in the vestiges. We used this phenotypic signature as a genetic proxy, testing for hindlimb directional asymmetry in six genera of squamate reptiles that independently evolved hindlimb reduction and for which genetic and developmental tools are not yet developed:Agamodon anguliceps,Bachia intermedia,Chalcides sepsoides,Indotyphlops braminus,Ophisaurus attenuatuas and O. ventralis, andTeius teyou. Significant asymmetry occurred in one taxon,Chalcides sepsoides, whose left‐side pelvis and femur vestiges were 18% and 64% larger than right‐side vestiges, respectively, suggesting modification inPitx1expression in that species.However, there was either right‐larger asymmetry or no directional asymmetry in the other five taxa, suggesting multiple developmental genetic pathways to hindlimb reduction in squamates and the vertebrates more generally.

 

In crown group tetrapods, individual digits are homologized in relation to a pentadactyl ground plan. However, testing hypotheses of digit homology is challenging because it is unclear whether digits represent distinct and conserved gene regulatory states. Here we show dramatic evolutionary dynamism in the gene expression profiles of digits, challenging the notion that five digits have conserved developmental identities across amniotes. Transcriptomics shows diversity in the patterns of gene expression differentiation of digits, although the anterior-most digit of the pentadactyl limb has a unique, conserved expression profile. Further, we identify a core set of transcription factors that are differentially expressed among the digits of amniote limbs; their spatial expression domains, however, vary between species. In light of these results, we reevaluate the frame shift hypothesis of avian wing evolution and conclude only the identity of the anterior-most digit has shifted position, suggesting a 1,3,4 digit identity in the bird wing.

 

Every stage of organismal life history is being challenged by global warming. Many species are already experiencing temperatures approaching their physiological limits; this is particularly true for ectothermic species, such as lizards. Embryos are markedly sensitive to thermal insult. Here, we demonstrate that temperatures currently experienced in natural nesting areas can modify gene expression levels and induce neural and craniofacial malformations in embryos of the lizard Anolis sagrei. Developmental abnormalities ranged from minor changes in facial structure to significant disruption of anterior face and forebrain. The first several days of postoviposition development are particularly sensitive to this thermal insult. These results raise new concern over the viability of ectothermic species under contemporary climate change. Herein, we propose and test a novel developmental hypothesis that describes the cellular and developmental origins of those malformations: cell death in the developing forebrain and abnormal facial induction due to disrupted Hedgehog signaling. Based on similarities in the embryonic response to thermal stress among distantly related species, we propose that this developmental hypothesis represents a common embryonic response to thermal insult among amniote embryos. Our results emphasize the importance of adopting a broad, multidisciplinary approach that includes both lab and field perspectives when trying to understand the future impacts of anthropogenic change on animal development.

 

One goal of evolutionary developmental biology is to understand the role of development in the origin of phenotypic novelty and convergent evolution. Geckos are an ideal system to study this topic, as they are species‐rich and exhibit a suite of diverse morphologies—many of which have independently evolved multiple times within geckos.

We characterized and discretized the embryonic development ofLepidodactylus lugubris—an all‐female, parthenogenetic gecko species. We also used soft‐tissue μCT to characterize the development of the brain and central nervous system, which is difficult to visualize using traditional microscopy techniques. Additionally, we sequenced and assembled a de novo transcriptome for a late‐stage embryo as a resource for generating future developmental tools. Herein, we describe the derived and conserved patterns ofL. lugubrisdevelopment in the context of squamate evolution and development.

This embryonic staging series, μCT data, and transcriptome together serve as critical enabling resources to study morphological evolution and development, the evolution and development of parthenogenesis, and other questions concerning vertebrate evolution and development in an emerging gecko model.