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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard.

Strongly selected characters can be transferred from one lineage to another with limited genetic exchange, resulting in asymmetric introgression and a mosaic genome in the receiving population. However, systems are rarely sufficiently well studied to link the pattern of introgression to its underlying process. Male common wall lizards in western Italy exhibit exaggeration of a suite of sexually selected characters that make them outcompete males from a distantly related lineage that lack these characters. This results in asymmetric hybridization and adaptive introgression of the suite of characters following secondary contact. We developed genomewide markers to infer the demographic history of gene flow between different genetic lineages, identify the spread of the sexually selected syndrome, and test the prediction that introgression should be asymmetric and heterogeneous across the genome. Our results show that secondary contact was accompanied by gene flow in both directions across most of the genome, but with approximately 3% of the genome showing highly asymmetric introgression in the predicted direction. Demographic simulations reveal that this asymmetric gene flow is more recent than the initial secondary contact, and the data suggest that the exaggerated male sexual characters originated within the Italian lineage and subsequently spread throughout this lineage before eventually reaching the contact zone. These results demonstrate that sexual selection can cause a suite of characters to spread throughout both closely and distantly related lineages with limited gene flow across the genome at large.

Avian predation intensity as a driver of clinal variation in colour morph frequency.

Phenotypic variation provides the framework for natural selection to work upon, enabling adaptive evolution. One of the most discernible manifestations of phenotypic variability is colour variation. When this variation is discrete, genetically based colour pattern morphs occur simultaneously within a population. Why and how colour polymorphisms are maintained is an evolutionary puzzle. Several evolutionary drivers have been hypothesized as influencing clinal patterns of morph frequency, with spatial variation in climate and predation being considered especially important. Despite this, no study has examined both of their roles simultaneously. The aims of this study were to: (a) examine the covariation of physiology, environmental variables and colouration at a local scale; and (b) determine if these factors and their interplay explain broad clinal variation in morph frequency. We used the lizard Liopholis whitii as a model system, as this species displays a discrete, heritable polymorphism for colour pattern (plain-backed, patterned morphs) whose morph frequency varies latitudinally. We measured reflectance, field activity temperatures and microhabitat structure to test for differences in crypsis, thermal biology and microhabitat selection of patterned and plain-backed morphs within a single population where colour morphs occur sympatrically. We then used data from the literature to perform a broad-scale analysis to identify whether these factors also explained the latitudinal variation of morph frequency in this species. At the local scale, plain-backed morphs were found to be less cryptic than patterned morphs while no other differences were detected in terms of thermal biology, dorsal reflectance and microhabitat use. At a broader scale, predation was the most influential factor mediating morph frequency across latitudes. However, the observed pattern of morph frequency is opposite to what the modelling results suggest in that the incidence of the least cryptic morph is highest where predation pressure is most severe. Clinal variation in the level of background matching between morphs or the potential reproductive advantage by the plain-backed morph may, instead, be driving the observed morph frequency. Together, these results provide key insights into the evolution of local adaptation as well as the ecological forces involved in driving the dynamics of colour polymorphism.

Maternal effects impact decision-making in a viviparous lizard.

Stressful conditions experienced during early development can have deleterious effects on offspring morphology, physiology and behaviour. However, few studies have examined how developmental stress influences an individual's cognitive phenotype. Using a viviparous lizard, we show that the availability of food resources to a mother during gestation influences a key component of her offspring's cognitive phenotype: their decision-making. Offspring from females who experienced low resource availability during gestation did better in an anti-predatory task that relied on spatial associations to guide their decisions, whereas offspring from females who experienced high resource availability during gestation did better in a foraging task that relied on colour associations to inform their decisions. This shows that the prenatal environment can influence decision-making in animals, a cognitive trait with functional implications later in life.

Mate familiarity and social learning in a monogamous lizard.

Social learning is thought to be advantageous as it allows an animal to gather information quickly without engaging in costly trial-and-error learning. However, animals should be selective about when and whom they learn from. Familiarity is predicted to positively influence an animal's reliance on social learning; yet, few studies have empirically tested this theory. We used a lizard (Liopholis whitii) that forms long-term monogamous pair bonds to examine the effects of partner familiarity on social learning in two novel foraging tasks, an association and a reversal task. We allowed female lizards to observe trained conspecifics that were either familiar (social mate) or unfamiliar execute these tasks and compared these two groups with control females that did not receive social information. Lizards preferentially relied on trial-and-error learning in the association task. In the reversal task, lizards that were demonstrated by familiar partners learnt in fewer trials compared to control lizards and made more correct choices. Our results provide some evidence for context-dependent learning with lizards differentiating between when they utilize social learning, and, to a limited degree, whom they learnt from. Understanding the role of the social context in which learning occurs provides important insights into the benefits of social learning and sociality more generally.

Climate and sex ratio variation in a viviparous lizard.

The extent to which key biological processes, such as sex determination, respond to environmental fluctuations is fundamental for assessing species' susceptibility to ongoing climate change. Few studies, however, address how climate affects offspring sex in the wild. We monitored two climatically distinct populations of the viviparous skink Niveoscincus ocellatus for 16 years, recording environmental temperatures, offspring sex and date of birth. We found strong population-specific effects of temperature on offspring sex, with female offspring more common in warm years at the lowland site but no effect at the highland site. In contrast, date of birth advanced similarly in response to temperature at both sites. These results suggest strong population-specific effects of temperature on offspring sex that are independent of climatic effects on other physiological processes. These results have significant implications for our understanding of the ecological and evolutionary consequences of variation in sex ratios under climate change.

Loss of genetic diversity and increased embryonic mortality in non-native lizard populations.

Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non-native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 non-native populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non-native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long-term viability. However, there was no statistical correlation between population-level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human-mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non-native species.

Climate-driven population divergence in sex-determining systems.

Sex determination is a fundamental biological process, yet its mechanisms are remarkably diverse. In vertebrates, sex can be determined by inherited genetic factors or by the temperature experienced during embryonic development. However, the evolutionary causes of this diversity remain unknown. Here we show that live-bearing lizards at different climatic extremes of the species' distribution differ in their sex-determining mechanisms, with temperature-dependent sex determination in lowlands and genotypic sex determination in highlands. A theoretical model parameterized with field data accurately predicts this divergence in sex-determining systems and the consequence thereof for variation in cohort sex ratios among years. Furthermore, we show that divergent natural selection on sex determination across altitudes is caused by climatic effects on lizard life history and variation in the magnitude of between-year temperature fluctuations. Our results establish an adaptive explanation for intra-specific divergence in sex-determining systems driven by phenotypic plasticity and ecological selection, thereby providing a unifying framework for integrating the developmental, ecological and evolutionary basis for variation in vertebrate sex determination.

Sexual selection drives asymmetric introgression in wall lizards.

Hybridisation is increasingly recognised as an important cause of diversification and adaptation. Here, we show how divergence in male secondary sexual characters between two lineages of the common wall lizard (Podarcis muralis) gives rise to strong asymmetries in male competitive ability and mating success, resulting in asymmetric hybridisation upon secondary contact. Combined with no negative effects of hybridisation on survival or reproductive characters in F1-hybrids, these results suggest that introgression should be asymmetric, resulting in the displacement of sexual characters of the sub-dominant lineage. This prediction was confirmed in two types of secondary contact, across a natural contact zone and in two introduced populations. Our study illustrates how divergence in sexually selected traits via male competition can determine the direction and extent of introgression, contributing to geographic patterns of genetic and phenotypic diversity.

Adaptive responses to cool climate promotes persistence of a non-native lizard.

Successful establishment and range expansion of non-native species often require rapid accommodation of novel environments. Here, we use common-garden experiments to demonstrate parallel adaptive evolutionary response to a cool climate in populations of wall lizards (Podarcis muralis) introduced from southern Europe into England. Low soil temperatures in the introduced range delay hatching, which generates directional selection for a shorter incubation period. Non-native lizards from two separate lineages have responded to this selection by retaining their embryos for longer before oviposition--hence reducing the time needed to complete embryogenesis in the nest--and by an increased developmental rate at low temperatures. This divergence mirrors local adaptation across latitudes and altitudes within widely distributed species and suggests that evolutionary responses to climate can be very rapid. When extrapolated to soil temperatures encountered in nests within the introduced range, embryo retention and faster developmental rate result in one to several weeks earlier emergence compared with the ancestral state. We show that this difference translates into substantial survival benefits for offspring. This should promote short- and long-term persistence of non-native populations, and ultimately enable expansion into areas that would be unattainable with incubation duration representative of the native range.