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Hox genes are a remarkable example of conservation in animal development and their nested expression along the head-to-tail axis orchestrates embryonic patterning. Early in vertebrate history, two duplications led to the emergence of four Hox clusters (A-D) and redundancy within paralog groups has been partially accommodated with gene losses. Here we conduct an inventory of squamate Hox genes using the genomes of 10 lizard and 7 snake species. Although the HoxC1 gene has been hypothesized to be lost in the amniote ancestor, we reveal that it is retained in lizards. In contrast, all snakes lack functional HoxC1 and -D12 genes. Varying levels of degradation suggest differences in the process of gene loss between the two genes. The vertebrate HoxC1 gene is prone to gene loss and its functional domains are more variable than those of other Hox1 genes. We describe for the first time the HoxC1 expression patterns in tetrapods. HoxC1 is broadly expressed during development in the diencephalon, the neural tube, dorsal root ganglia, and limb buds in two lizard species. Our study emphasizes the value of revisiting Hox gene repertoires by densely sampling taxonomic groups and its feasibility owing to growing sequence resources in evaluating gene repertoires across taxa.

The Mediterranean basin is a hotspot of biodiversity, fuelled by climatic oscillation and geological change over the past 20 million years. Wall lizards of the genus Podarcis are among the most abundant, diverse, and conspicuous Mediterranean fauna. Here, we unravel the remarkably entangled evolutionary history of wall lizards by sequencing genomes of 34 major lineages covering 26 species. We demonstrate an early (>11 MYA) separation into two clades centred on the Iberian and Balkan Peninsulas, and two clades of Mediterranean island endemics. Diversification within these clades was pronounced between 6.5–4.0 MYA, a period spanning the Messinian Salinity Crisis, during which the Mediterranean Sea nearly dried up before rapidly refilling. However, genetic exchange between lineages has been a pervasive feature throughout the entire history of wall lizards. This has resulted in a highly reticulated pattern of evolution across the group, characterised by mosaic genomes with major contributions from two or more parental taxa. These hybrid lineages gave rise to several of the extant species that are endemic to Mediterranean islands. The mosaic genomes of island endemics may have promoted their extraordinary adaptability and striking diversity in body size, shape and colouration, which have puzzled biologists for centuries.

The survival prospects of threatened species or populations can sometimes be improved by adaptive change. Such evolutionary rescue is particularly relevant when the threat comes from changing environments, or when long-term population persistence requires range expansion into new habitats. Conservation biologists are therefore often interested in whether or not populations or lineages show a disposition for adaptive evolution, that is, if they are evolvable. Here, we discuss four alternative perspectives that target different causes of evolvability and outline some of the key challenges those perspectives are designed to address. Standing genetic variation provides one familiar estimate of evolvability. Yet, the mere presence of genetic variation is often insufficient to predict if a population will adapt, or how it will adapt. The reason is that adaptive change not only depends on genetic variation, but also on the extent to which this genetic variation can be realized as adaptive phenotypic variation. This requires attention to developmental systems and how plasticity influences evolutionary potential. Finally, we discuss how a better understanding of the different factors that contribute to evolvability can be exploited in conservation practice.

Anolis lizards originated in continental America but have colonized the Greater Antillean islands and recolonized the mainland, resulting in three major groups (Primary and Secondary Mainland and Greater Antillean). The adaptive radiation in the Greater Antilles has famously resulted in the repeated evolution of ecomorphs. Yet, it remains poorly understood to what extent this island radiation differs from diversification on the mainland. Here, we demonstrate that the evolutionary modularity between girdles and limbs is fundamentally different in the Greater Antillean and Primary Mainland Anolis. This is consistent with ecological opportunities on islands driving the adaptive radiation along distinct evolutionary trajectories. However, Greater Antillean Anolis share evolutionary modularity with the group that recolonized the mainland, demonstrating a persistent phylogenetic inertia. A comparison of these two groups support an increased morphological diversity and faster and more variable evolutionary rates on islands. These macroevolutionary trends of the locomotor skeleton in Anolis illustrate that ecological opportunities on islands can have lasting effects on morphological diversification., Both ecological opportunity and phenotypic modularity have been suggested to facilitate adaptive radiations. Feiner et al. show that Anolis lizards evolved a new modularity structure in their island adaptive radiation, but that this modularity did not produce the same extreme diversification when Anolis returned to the mainland.

Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress.

Populations adapting independently to the same environment provide important insights into the repeatability of evolution at different levels of biological organization. In the 20th century, common wall lizards (Podarcis muralis) from southern and western Europe were introduced to England, north of their native range. Nonnative populations of both lineages have adapted to the shorter season and lower egg incubation temperature by increasing the absolute rate of embryonic development. Here, we tested if this adaptation is accompanied by signatures of directional selection in the transcriptomes of early embryos and, if so, if nonnative populations show adaptive convergence. Embryos from nonnative populations exhibited gene expression profiles consistent with directional selection following introduction, but different genes were affected in the two lineages. Despite this, the functional enrichment of genes that changed their expression following introduction showed substantial similarity between lineages, and was consistent with mechanisms that should promote developmental rate. Moreover, the divergence between nonnative and native populations was enriched for genes that were temperature-responsive in native populations. These results indicate that small populations are able to adapt to new climatic regimes, but the means by which they do so may largely be determined by founder effects and other sources of genetic drift.

Hybrid zones provide insights into the evolution of reproductive isolation. Sexual selection can contribute to the evolution of reproductive barriers, but it remains poorly understood how sexual traits impact gene flow in secondary contact. Here, we show that a recently evolved suite of sexual traits that function in male-male competition mediates gene flow between two lineages of wall lizards (Podarcis muralis). Gene flow was relatively low and asymmetric in the presence of exaggerated male morphology and coloration compared to when the lineages share the ancestral phenotype. Putative barrier loci were enriched in genomic regions that were highly differentiated between the two lineages and showed low concordance between the transects. The exception was a consistently low genetic exchange around ATXN1, a gene that modulates social behavior. We suggest that this gene may contribute to the male mate preferences that are known to cause lineage-assortative mating in this species. Although female choice modulates the degree of reproductive isolation in a variety of taxa, wall lizards demonstrate that both male-male competition and male mate choice can contribute to the extent of gene flow between lineages.

The radiation of Anolis lizards in the Caribbean is associated with a diversification of the functional match between morphology, habitat use, and locomotor performance. It has been hypothesized that the microhabitat a lizard is reared in can achieve a similar fit of form and function within a species. This predicts that plasticity in the locomotor apparatus is accompanied by changes in perching behavior or improved locomotor performance. To test this, we raised juveniles of two species (Anolis sagrei and Anolis carolinensis) on either broad or narrow surfaces and examined perching behavior and locomotor performance as well as the shape of the pectoral and pelvic girdles, limb length, and thickness of the long bones. Perching behavior was not affected by the habitat surface experienced during ontogeny. However, individuals raised on broad surfaces showed better locomotor performance on broad surfaces, and the magnitude of the effect was as large as the difference between the two species. Both species showed modifications of pectoral and pelvic shape, but only A. carolinensis developed longer limbs on broad surfaces. However, these morphological adjustments induced by physical activity did not explain why lizards raised on broad surfaces performed better. Thus, it appears that early-life experiences can affect both the morphology of the locomotor apparatus and locomotor performance in Anolis lizards, without the two being functionally connected.

Developmental plasticity looks like a promising bridge between ecological and developmental perspectives on evolution. Yet, there is no consensus on whether plasticity is part of the explanation for adaptive evolution or an optional "add-on" to genes and natural selection. Here, we suggest that these differences in opinion are caused by differences in the simplifying assumptions, and particular idealizations, that enable evolutionary explanation. We outline why idealizations designed to explain evolution through natural selection prevent an understanding of the role of development, and vice versa. We show that representing plasticity as a reaction norm conforms with the idealizations of selective explanations, which can give the false impression that plasticity has no explanatory power for adaptive evolution. Finally, we use examples to illustrate why evolutionary explanations that include developmental plasticity may in fact be more satisfactory than explanations that solely refer to genes and natural selection.

The vertebrate gene repertoire is characterized by “cryptic” genes whose identification has been hampered by their absence from the genomes of well-studied species. One example is the Bmp16 gene, a paralog of the developmental key genes Bmp2 and -4. We focus on the Bmp2/4/16 group of genes to study the evolutionary dynamics following gen(om)e duplications with special emphasis on the poorly studied Bmp16 gene. We reveal the presence of Bmp16 in chondrichthyans in addition to previously reported teleost fishes and reptiles. Using comprehensive, vertebrate-wide gene sampling, our phylogenetic analysis complemented with synteny analyses suggests that Bmp2, -4 and -16 are remnants of a gene quartet that originated during the two rounds of whole-genome duplication (2R-WGD) early in vertebrate evolution. We confirm that Bmp16 genes were lost independently in at least three lineages (mammals, archelosaurs and amphibians) and report that they have elevated rates of sequence evolution. This finding agrees with their more “flexible” deployment during development; while Bmp16 has limited embryonic expression domains in the cloudy catshark, it is broadly expressed in the green anole lizard. Our study illustrates the dynamics of gene family evolution by integrating insights from sequence diversification, gene repertoire changes, and shuffling of expression domains.

Phylogenetic approaches are indispensable in any comparative molecular study involving multiple species. These approaches are in increasing demand as the amount and availability of DNA sequence information continues to increase exponentially, even for organisms that were previously not extensively studied. Without the sound application of phylogenetic concepts and knowledge, one can be misled when attempting to infer ancestral character states as well as the timing and order of evolutionary events, both of which are frequently exerted in evolutionary developmental biology. The ignorance of phylogenetic approaches can also impact non-evolutionary studies and cause misidentification of the target gene or protein to be examined in functional characterization. This review aims to promote tree-thinking in evolutionary conjecture and stress the importance of a sense of time scale in cross-species comparisons, in order to enhance the understanding of phylogenetics in all biological fields including developmental biology. To this end, molecular phylogenies of several developmental regulatory genes, including those denoted as "cryptic pan-vertebrate genes", are introduced as examples.

Transposable elements (TEs) are DNA sequences that can insert elsewhere in the genome and modify genome structure and gene regulation. The role of TEs in evolution is contentious. One hypothesis posits that TE activity generates genomic incompatibilities that can cause reproductive isolation between incipient species. This predicts that TEs will accumulate during speciation events. Here, I tested the prediction that extant lineages with a relatively high rate of speciation have a high number of TEs in their genomes. I sequenced and analysed the TE content of a marker genomic region (Hoxclusters) inAnolislizards, a classic case of an adaptive radiation. Unlike other vertebrates, including closely related lizards,Anolislizards have high numbers of TEs in theirHoxclusters, genomic regions that regulate development of the morphological adaptations that characterize habitat specialists in these lizards. Following a burst of TE activity in the lineage leading to extantAnolis, TEs have continued to accumulate during or after speciation events, resulting in a positive relationship between TE density and lineage speciation rate. These results are consistent with the prediction that TE activity contributes to adaptive radiation by promoting speciation. Although there was no evidence that TE densityper seis associated with ecological morphology, the activity of TEs inHoxclusters could have been a rich source for phenotypic variation that may have facilitated the rapid parallel morphological adaptation to microhabitats seen in extantAnolislizards.