Adaptive introgression reveals the genetic basis of a sexually selected syndrome in wall lizards.

The joint expression of particular colors, morphologies, and behaviors is a common feature of adaptation, but the genetic basis for such "phenotypic syndromes" remains poorly understood. Here, we identified a complex genetic architecture associated with a sexually selected syndrome in common wall lizards, by capitalizing on the adaptive introgression of coloration and morphology into a distantly related lineage. Consistent with the hypothesis that the evolution of phenotypic syndromes in vertebrates is facilitated by developmental linkage through neural crest cells, most of the genes associated with the syndrome are involved in neural crest cell regulation. A major locus was a ~400-kb region, characterized by standing structural genetic variation and previously implied in the evolutionary innovation of coloration and beak size in birds. We conclude that features of the developmental and genetic architecture contribute to maintaining trait integration, facilitating the extensive and rapid introgressive spread of suites of sexually selected characters.

Sex and early-life conditions shape telomere dynamics in an ectotherm.

Telomeres, the repetitive DNA regions that protect the ends of chromosomes, and their shortening have been linked to key life history trade-offs among growth, reproduction and lifespan. In contrast to most endotherms, many ectotherms can compensate for telomere shortening throughout life by upregulation of telomerase in somatic tissues. However, during development, marked by rapid growth and an increased sensitivity to extrinsic factors, the upregulation of telomerase may be overwhelmed, resulting in long-term impacts on telomere dynamics. In ectotherms, one extrinsic factor that may play a particularly important role in development is temperature. Here, we investigated the influence of developmental temperature and sex on early-life telomere dynamics in an oviparous ectotherm, Lacerta agilis. While there was no effect of developmental temperature on telomere length at hatching, there were subsequent effects on telomere maintenance capacity, with individuals incubated at warm temperatures exhibiting less telomere maintenance compared with cool-incubated individuals. Telomere dynamics were also sexually dimorphic, with females having longer telomeres and greater telomere maintenance compared with males. We suggest that selection drives this sexual dimorphism in telomere maintenance, in which females maximise their lifetime reproductive success by investing in traits promoting longevity such as maintenance, while males invest in short-term reproductive gains through a polygynous mating behaviour. These early-life effects, therefore, have the potential to mediate life-long changes to life histories.

Maternal behavioral thermoregulation facilitated evolutionary transitions from egg laying to live birth.

Live birth is a key innovation that has evolved from egg-laying ancestors over 100 times in reptiles. However, egg-laying lizards and snakes can have preferred body temperatures that are lethal to developing embryos, which should select against prolonged egg retention. Here, we demonstrate that thermal mismatches between mothers and offspring are widespread across the squamate phylogeny. This mismatch is resolved by gravid females adjusting their body temperature towards the thermal optimum of their embryos. We find that the same response occurs in both live-bearing and egg-laying species, despite the latter only retaining embryos during the early stages of development. Importantly, phylogenetic reconstructions suggest this thermoregulatory behavior in gravid females evolved in egg-laying species prior to the evolution of live birth. Maternal thermoregulatory behavior, therefore, bypasses the constraints imposed by a slowly evolving thermal physiology and has likely been a key facilitator in the repeated transition to live birth.

Context-dependent thermolability of sex determination in a lacertid lizard with heteromorphic sex chromosomes.

Developmental conditions can profoundly impact key life history traits of the individual. In cases where offspring sex is driven by developmental reaction norms, permanent changes to the phenotype can fundamentally alter life history trajectories. Sex determination mechanisms in reptiles are remarkably diverse, including well-characterised genetic and temperature-dependent sex determination. In rarer, but increasingly more commonly documented cases, sex can also be determined by a combination of the two, with temperature overriding the genetically determined sex. Thus, sex-by-temperature interactions is a mechanism that can be contextually labile, where reaction norms of sex against developmental environment might only be observable under certain conditions. We examine the effects of incubation temperature on hatchling sex in an oviparous lizard with clearly defined heteromorphic sex chromosomes presumed to determine sex solely on a genetic basis. We also test the repeatability of our results by replicating incubation experiments across 3 years. We show that warmer temperatures may override chromosomal sex and cause an overproduction of daughters. However, this effect was inconsistent among years, with high temperature only resulting in a daughter-significant bias in one year. Warm-incubated daughters were more efficient at converting yolk into tissue, which would allow for greater resource allocation to other fitness-related processes, such as growth. This suggests that thermolabile sex determination could be a trait under selection. More energy-efficient embryos also produced faster-growing offspring, suggesting that energy utilization patterns of the embryo were maintained into the juvenile stage, which could have important implications for the ontogenetic development and evolution of life histories.

Thermal Plasticity in Behavioral Traits Mediates Mating and Reproductive Dynamics in an Ectotherm.

AbstractEnvironmental temperatures potentially influence reproductive performance and sexual selection by restricting opportunities for activity. However, explicit tests of the behavioral mechanisms linking thermal variation to mating and reproductive performance are rare. We address this gap in a temperate lizard by combining social network analysis with molecular pedigree reconstruction in a large-scale thermal manipulation experiment. Populations exposed to cool thermal regimes presented fewer high-activity days compared with populations exposed to a warmer regime. While plasticity in thermal activity responses in males masked overall differences in activity levels, prolonged restriction nevertheless affected the timing and consistency of male-female interactions. Females were less capable than males of compensating for lost activity time under cold stress, and less active females in this group were significantly less likely to reproduce. While sex-biased activity suppression appeared to limit male mating rates, this did not correspond to a heightened intensity of sexual selection or shifts in the targets of sexual selection. In many populations facing thermal activity restriction, sexual selection on males may play a limited role relative to other thermal performance traits in facilitating adaptation.

Sex reversal explains some, but not all, climate-mediated sex ratio variation within a viviparous reptile.

Evolutionary transitions in sex-determining systems have occurred frequently yet understanding how they occur remains a major challenge. In reptiles, transitions from genetic to temperature-dependent sex determination can occur if the gene products that determine sex evolve thermal sensitivity, resulting in sex-reversed individuals. However, evidence of sex reversal is limited to oviparous reptiles. Here we used thermal experiments to test whether sex reversal is responsible for differences in sex determination in a viviparous reptile, Carinascincus ocellatus, a species with XY sex chromosomes and population-specific sex ratio response to temperature. We show that sex reversal is occurring and that its frequency is related to temperature. Sex reversal was unidirectional (phenotypic males with XX genotype) and observed in both high- and low-elevation populations. We propose that XX-biased genotypic sex ratios could produce either male- or female-biased phenotypic sex ratios as observed in low-elevation C. ocellatus under variable rates of XX sex reversal. We discuss reasons why sex reversal may not influence sex ratios at high elevation. Our results suggest that the mechanism responsible for evolutionary transitions from genotypic to temperature-dependent sex determination is more complex than can be explained by a single process such as sex reversal.

Impact of fluctuating developmental temperatures on phenotypic traits in reptiles: a meta-analysis.

During the vulnerable stages of early life, most ectothermic animals experience hourly and diel fluctuations in temperature as air temperatures change. While we know a great deal about how different constant temperatures impact the phenotypes of developing ectotherms, we know remarkably little about the impacts of temperature fluctuations on the development of ectotherms. In this study, we used a meta-analytic approach to compare the mean and variance of phenotypic outcomes from constant and fluctuating incubation temperatures across reptile species. We found that fluctuating temperatures provided a small benefit (higher hatching success and shorter incubation durations) at cool mean temperatures compared with constant temperatures, but had a negative effect at warm mean temperatures. In addition, more extreme temperature fluctuations led to greater reductions in embryonic survival compared with moderate temperature fluctuations. Within the limited data available from species with temperature-dependent sex determination, embryos had a higher chance of developing as female when developing in fluctuating temperatures compared with those developing in constant temperatures. With our meta-analytic approach, we identified average mean nest temperatures across all taxa where reptiles switch from receiving benefits to incurring costs when incubation temperatures fluctuate. More broadly, our study indicates that the impact of fluctuating developmental temperature on some phenotypes in ectothermic taxa are likely to be predictable via integration of developmental temperature profiles with thermal performance curves.

Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard.

Species distributed across climatic gradients will typically experience spatial variation in selection, but gene flow can prevent such selection from causing population genetic differentiation and local adaptation. Here, we studied genomic variation of 415 individuals across 34 populations of the common wall lizard (Podarcis muralis) in central Italy. This species is highly abundant throughout this region and populations belong to a single genetic lineage, yet there is extensive phenotypic variation across climatic regimes. We used redundancy analysis to, first, quantify the effect of climate and geography on population genomic variation in this region and, second, to test if climate consistently sorts specific alleles across the landscape. Climate explained 5% of the population genomic variation across the landscape, about half of which was collinear with geography. Linear models and redundancy analyses identified loci that were significantly differentiated across climatic regimes. These loci were distributed across the genome and physically associated with genes putatively involved in thermal tolerance, regulation of temperature-dependent metabolism and reproductive activity, and body colouration. Together, these findings suggest that climate can exercise sufficient selection in lizards to promote genetic differentiation across the landscape in spite of high gene flow.

Population Genomics of Wall Lizards Reflects the Dynamic History of the Mediterranean Basin.

The Mediterranean Basin has experienced extensive change in geology and climate over the past six million years. Yet, the relative importance of key geological events for the distribution and genetic structure of the Mediterranean fauna remains poorly understood. Here, we use population genomic and phylogenomic analyses to establish the evolutionary history and genetic structure of common wall lizards (Podarcis muralis). This species is particularly informative because, in contrast to other Mediterranean lizards, it is widespread across the Iberian, Italian, and Balkan Peninsulas, and in extra-Mediterranean regions. We found strong support for six major lineages within P. muralis, which were largely discordant with the phylogenetic relationship of mitochondrial DNA. The most recent common ancestor of extant P. muralis was likely distributed in the Italian Peninsula, and experienced an "Out-of-Italy" expansion following the Messinian salinity crisis (∼5 Mya), resulting in the differentiation into the extant lineages on the Iberian, Italian, and Balkan Peninsulas. Introgression analysis revealed that both inter- and intraspecific gene flows have been pervasive throughout the evolutionary history of P. muralis. For example, the Southern Italy lineage has a hybrid origin, formed through admixture between the Central Italy lineage and an ancient lineage that was the sister to all other P. muralis. More recent genetic differentiation is associated with the onset of the Quaternary glaciations, which influenced population dynamics and genetic diversity of contemporary lineages. These results demonstrate the pervasive role of Mediterranean geology and climate for the evolutionary history and population genetic structure of extant species.

Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers.

Maternal stress during gestation has the potential to affect offspring development via changes in maternal physiology, such as increases in circulating levels of glucocorticoid hormones that are typical after exposure to a stressor. While the effects of elevated maternal glucocorticoids on offspring phenotype (i.e., "glucocorticoid-mediated maternal effects") have been relatively well established in laboratory studies, it remains poorly understood how strong and consistent such effects are in natural populations. Using a meta-analysis of studies of wild mammals, birds, and reptiles, we investigate the evidence for effects of elevated maternal glucocorticoids on offspring phenotype and investigate key moderators that might influence the strength and direction of these effects. In particular, we investigate the potential importance of reproductive mode (viviparity vs. oviparity). We show that glucocorticoid-mediated maternal effects are stronger, and likely more deleterious, in mammals and viviparous squamate reptiles compared with birds, turtles, and oviparous squamates. No other moderators (timing and type of manipulation, age at offspring measurement, or type of trait measured) were significant predictors of the strength or direction of the phenotypic effects on offspring. These results provide evidence that the evolution of a prolonged physiological association between embryo and mother sets the stage for maladaptive, or adaptive, prenatal stress effects in vertebrates driven by glucocorticoid elevation.

Climate Shapes the Geographic Distribution and Introgressive Spread of Color Ornamentation in Common Wall Lizards.

AbstractClimate can exert an effect on the strength of sexual selection, but empirical evidence is limited. Here, we tested whether climate predicts the geographic distribution and introgressive spread of sexually selected male color ornamentation across 114 populations of the common wall lizard, Podarcis muralis. Coloration was highly structured across the landscape and did not reflect genetic differentiation. Instead, color ornamentation was consistently exaggerated in hot and dry environments, suggesting that climate-driven selection maintains geographic variation in spite of gene flow. Introgression of color ornamentation into a distantly related lineage appears to be ongoing and was particularly pronounced in warm climates with wet winters and dry summers. Combined, these results suggest that sexual ornamentation is consistently favored in climates that allow a prolonged reproductive season and high and reliable opportunities for lizard activity. This pattern corroborates theoretical predictions that such climatic conditions reduce the temporal clustering of receptive females and increase male-male competition, resulting in strong sexual selection. In summary, we provide compelling evidence for the importance of climate for the evolution of color ornamentation, and we demonstrate that geographic variation in the strength of sexual selection influences introgression of this phenotype.

The thermal environment as a moderator of social evolution.

Animal sociality plays a crucial organisational role in evolution. As a result, understanding the factors that promote the emergence, maintenance, and diversification of animal societies is of great interest to biologists. Climate is among the foremost ecological factors implicated in evolutionary transitions in social organisation, but we are only beginning to unravel the possible mechanisms and specific climatic variables that underlie these associations. Ambient temperature is a key abiotic factor shaping the spatio-temporal distribution of individuals and has a particularly strong influence on behaviour. Whether such effects play a broader role in social evolution remains to be seen. In this review, we develop a conceptual framework for understanding how thermal effects integrate into pathways that mediate the opportunities, nature, and context of social interactions. We then implement this framework to discuss the capacity for temperature to initiate organisational changes across three broad categories of social evolution: group formation, group maintenance, and group elaboration. For each category, we focus on pivotal traits likely to have underpinned key social transitions and explore the potential for temperature to affect changes in these traits by leveraging empirical examples from the literature on thermal and behavioural ecology. Finally, we discuss research directions that should be prioritised to understand the potentially constructive and/or destructive effects of future warming on the origins, maintenance, and diversification of animal societies.

Extensive introgression and mosaic genomes of Mediterranean endemic lizards.

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.

Temporal variation in thermal plasticity in a free-ranging subalpine lizard.

Thermally variable environments are particularly challenging for ectotherms as physiological functions are thermo-dependent. As a consequence, ectotherms in highly seasonal environments are predicted to have greater thermal plasticity. However, much of our understanding of thermal plasticity comes from controlled experiments in a laboratory setting. Relatively fewer studies investigate thermal plasticity in free-ranging animals living in their natural environment. We investigated the presence of thermal plasticity within a single activity season in adult males of a natural high elevation population of White's skink (Liopholis whitii) in south-eastern Australia. This species lives in a permanent home site (rock crevice and/or burrow), facilitating the repeated capture of the same individuals across the activity season. We monitored the thermal variation across the field site and over the activity season, and tested thermal tolerances and performance of male L. whitii on three occasions across their activity season. Maximum and average temperatures varied across the field site, and temperatures gradually increased across the study period. Evidence of temporal plasticity was identified in the critical thermal minimum and thermal tolerance breadth, but not in the critical thermal maximum. Thermal performance was also found to be plastic, but no temporal patterns were evident. Our temporal plasticity results are consistent which much of the previous literature, but this is one of the first studies to identify these patterns in a free-ranging population. In addition, our results indicate that performance may be more plastic than previous literature suggests. Overall, our study highlights the need to pair laboratory and field studies in order to understand thermal plasticity in an ecologically relevant context.

Degrees of change: between and within population variation in thermal reaction norms of phenology in a viviparous lizard.

As the earth warms, populations will be faced with novel environments to which they may not be adapted. In the short term, populations can be buffered against the negative effects, or maximize the beneficial effects, of such environmental change via phenotypic plasticity and, in the longer term, via adaptive evolution. However, the extent and direction of these population-level responses will be dependent on the degree to which responses vary among the individuals within them (i.e., within population variation in plasticity), which is, itself, likely to vary among populations. Despite this, we have estimates of among-individual variation in plastic responses across multiple populations for only a few systems. This lack of data limits our ability to predict the consequences of environmental change for population and species persistence accurately. Here, we utilized a 16-yr data set from climatically distinct populations of the viviparous skink Niveoscincus ocellatus tracking over 1,200 litters from more than 600 females from each population to examine inter- and intrapopulation variability in the response of parturition date to environmental temperature. We found that these populations share a common population-mean reaction norm but differ in the degree to which reaction norms vary among individuals. These results suggest that even where populations share a common mean-level response, we cannot assume that they will be affected similarly by altered environmental conditions. If we are to assess how changing climates will impact species and populations accurately, we require estimates of how plastic responses vary both among and within populations.

Spatial variation in gene flow across a hybrid zone reveals causes of reproductive isolation and asymmetric introgression in wall lizards.

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.

Developmental Biology: Embryonic Movement Influences Sex Determination in a Turtle.

Many ectotherms behaviourally thermoregulate to maintain their body temperatures within an optimal range. A new study suggests that turtle embryos developing inside eggs also have this capacity, and that this can have significant implications for sex determination.

Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard.

Reptiles use pterin and carotenoid pigments to produce yellow, orange, and red colors. These conspicuous colors serve a diversity of signaling functions, but their molecular basis remains unresolved. Here, we show that the genomes of sympatric color morphs of the European common wall lizard (Podarcis muralis), which differ in orange and yellow pigmentation and in their ecology and behavior, are virtually undifferentiated. Genetic differences are restricted to two small regulatory regions near genes associated with pterin [sepiapterin reductase (SPR)] and carotenoid [beta-carotene oxygenase 2 (BCO2)] metabolism, demonstrating that a core gene in the housekeeping pathway of pterin biosynthesis has been coopted for bright coloration in reptiles and indicating that these loci exert pleiotropic effects on other aspects of physiology. Pigmentation differences are explained by extremely divergent alleles, and haplotype analysis revealed abundant transspecific allele sharing with other lacertids exhibiting color polymorphisms. The evolution of these conspicuous color ornaments is the result of ancient genetic variation and cross-species hybridization.

Low food availability during gestation enhances offspring post-natal growth, but reduces survival, in a viviparous lizard.

The environment experienced by a mother can have profound effects on the fitness of her offspring (i.e., maternal effects). Maternal effects can be adaptive when the developmental environments experienced by offspring promote phenotypes that provide fitness benefits either via matching offspring phenotype to the post-developmental environment (also known as anticipatory maternal effects) or through direct effects on offspring growth and survival. We tested these hypotheses in a viviparous lizard using a factorial experimental design in which mothers received either high or low amounts of food during gestation, and resultant offspring were raised on either high or low amounts of food post-birth. We found no effect of food availability during gestation on reproductive traits of mothers or offspring traits at birth. However, offspring from mothers who received low food during gestation exhibited a greater increase in condition in the post-birth period, suggesting some form of priming of offspring by mothers to cope with an anticipated poor environment after birth. Offspring that received low food during gestation were also more likely to die, suggesting a trade-off for this accelerated growth. There were also significant effects of post-birth food availability on offspring snout-vent length and body condition growth, with offspring with high food availability post birth doing better. However, the effects of the pre- and post-natal resource evnironment on offspring growth were independent on one another, therefore, providing no support for the presence of anticipatory maternal effects in the traditional sense.

The diversity of population responses to environmental change.

The current extinction and climate change crises pressure us to predict population dynamics with ever-greater accuracy. Although predictions rest on the well-advanced theory of age-structured populations, two key issues remain poorly explored. Specifically, how the age-dependency in demographic rates and the year-to-year interactions between survival and fecundity affect stochastic population growth rates. We use inference, simulations and mathematical derivations to explore how environmental perturbations determine population growth rates for populations with different age-specific demographic rates and when ages are reduced to stages. We find that stage- vs. age-based models can produce markedly divergent stochastic population growth rates. The differences are most pronounced when there are survival-fecundity-trade-offs, which reduce the variance in the population growth rate. Finally, the expected value and variance of the stochastic growth rates of populations with different age-specific demographic rates can diverge to the extent that, while some populations may thrive, others will inevitably go extinct.