Genetic diversity, phylogenetic position, and co-phylogenetic relationships of Karyolysus, a common blood parasite of lizards in the western Mediterranean.

The genus Karyolysus was originally proposed to accommodate blood parasites of lacertid lizards in Western Europe. However, recent phylogenetic analyses suggested an inconclusive taxonomic position of these parasites of the order Adeleorina based on the available genetic information. Inconsistencies between molecular phylogeny, morphology, and/or life cycles can reflect lack of enough genetic information of the target group. We therefore surveyed 28 localities and collected blood samples from 828 lizards of 23 species including lacertids, skinks, and geckoes in the western Mediterranean, North Africa, and Macaronesia, where species of Karyolysus and other adeleorine parasites have been described. We combined molecular and microscopic methods to analyze the samples, including those from the host type species and the type locality of Karyolysus bicapsulatus. The phylogenetic relationship of these parasites was analyzed based on the 18S rRNA gene and the co-phylogenetic relationship with their vertebrate hosts was reconstructed. We molecularly detected adeleorine parasites in 37.9% of the blood samples and found 22 new parasite haplotypes. A phylogenetic reconstruction with 132 sequences indicated that 20 of the newly detected haplotypes clustered in a well-supported clade with another 18 sequences that included Karyolysus galloti and Karyolysus lacazei. Morphological evidence also supported that K. bicapsulatus clustered in this monophyletic clade. These results supported the taxonomic validity of the genus. In addition, we found some parasite haplotypes that infected different lizard host genera with ancient diverging histories, which suggested that Karyolysus is less host-specific than other blood parasites of lizards in the region. A co-phylogenetic analysis supported this interpretation because no significant co-speciation signal was shown between Karyolysus and lizard hosts.

Ambra1 haploinsufficiency in CD1 mice results in metabolic alterations and exacerbates age-associated retinal degeneration.

Macroautophagy/autophagy is a key process in the maintenance of cellular homeostasis. The age-dependent decline in retinal autophagy has been associated with photoreceptor degeneration. Retinal dysfunction can also result from damage to the retinal pigment epithelium (RPE), as the RPE-retina constitutes an important metabolic ecosystem that must be finely tuned to preserve visual function. While studies of mice lacking essential autophagy genes have revealed a predisposition to retinal degeneration, the consequences of a moderate reduction in autophagy, similar to that which occurs during physiological aging, remain unclear. Here, we described a retinal phenotype consistent with accelerated aging in mice carrying a haploinsufficiency for Ambra1, a pro-autophagic gene. These mice showed protein aggregation in the retina and RPE, metabolic underperformance, and premature vision loss. Moreover, Ambra1+/gt mice were more prone to retinal degeneration after RPE stress. These findings indicate that autophagy provides crucial support to RPE-retinal metabolism and protects the retina against stress and physiological aging.Abbreviations : 4-HNE: 4-hydroxynonenal; AMBRA1: autophagy and beclin 1 regulator 1, AMD: age-related macular degeneration;; GCL: ganglion cell layer; GFAP: glial fibrillary acidic protein; GLUL: glutamine synthetase/glutamate-ammonia ligase; HCL: hierarchical clustering; INL: inner nuclear layer; IPL: inner plexiform layer; LC/GC-MS: liquid chromatography/gas chromatography-mass spectrometry; MA: middle-aged; MTDR: MitoTracker Deep Red; MFI: mean fluorescence intensity; NL: NH4Cl and leupeptin; Nqo: NAD(P)H quinone dehydrogenase; ONL: outer nuclear layer; OPL: outer plexiform layer; OP: oscillatory potentials; OXPHOS: oxidative phosphorylation; PCR: polymerase chain reaction; PRKC/PKCα: protein kinase C; POS: photoreceptor outer segment; RGC: retinal ganglion cells; RPE: retinal pigment epithelium; SI: sodium iodate; TCA: tricarboxylic acid.

Precipitation predictability affects intra- and trans-generational plasticity and causes differential selection on root traits of Papaver rhoeas.

Climate forecasts show that in many regions the temporal distribution of precipitation events will become less predictable. Root traits may play key roles in dealing with changes in precipitation predictability, but their functional plastic responses, including transgenerational processes, are scarcely known. We investigated root trait plasticity of Papaver rhoeas with respect to higher versus lower intra-seasonal and inter-seasonal precipitation predictability (i.e., the degree of temporal autocorrelation among precipitation events) during a four-year outdoor multi-generation experiment. We first tested how the simulated predictability regimes affected intra-generational plasticity of root traits and allocation strategies of the ancestors, and investigated the selective forces acting on them. Second, we exposed three descendant generations to the same predictability regime experienced by their mothers or to a different one. We then investigated whether high inter-generational predictability causes root trait differentiation, whether transgenerational root plasticity existed and whether it was affected by the different predictability treatments. We found that the number of secondary roots, root biomass and root allocation strategies of ancestors were affected by changes in precipitation predictability, in line with intra-generational plasticity. Lower predictability induced a root response, possibly reflecting a fast-acquisitive strategy that increases water absorbance from shallow soil layers. Ancestors' root traits were generally under selection, and the predictability treatments did neither affect the strength nor the direction of selection. Transgenerational effects were detected in root biomass and root weight ratio (RWR). In presence of lower predictability, descendants significantly reduced RWR compared to ancestors, leading to an increase in performance. This points to a change in root allocation in order to maintain or increase the descendants' fitness. Moreover, transgenerational plasticity existed in maximum rooting depth and root biomass, and the less predictable treatment promoted the lowest coefficient of variation among descendants' treatments in five out of six root traits. This shows that the level of maternal predictability determines the variation in the descendants' responses, and suggests that lower phenotypic plasticity evolves in less predictable environments. Overall, our findings show that roots are functional plastic traits that rapidly respond to differences in precipitation predictability, and that the plasticity and adaptation of root traits may crucially determine how climate change will affect plants.

Global changes explain the long-term demographic trend of the Eurasian common lizard (Squamata: Lacertidae).

The demographic trend of a species depends on the dynamics of its local populations, which can be compromised by local or by global phenomena. However, the relevance of local and global phenomena has rarely been investigated simultaneously. Here, we tested whether local phenomena compromised a species' demographic trend using the Eurasian common lizard Zootoca vivipara, the terrestrial reptile exhibiting the widest geographic distribution, as a model species. We analyzed the species' ancient demographic trend using genetic data from its 6 allopatric genetic clades and tested whether its demographic trend mainly depended on single clades or on global phenomena. Zootoca vivipara's effective population size increased since 2.3 million years ago and started to increase steeply and continuously from 0.531 million years ago. Population growth rate exhibited 2 maxima, both occurring during global climatic changes and important vegetation changes on the northern hemisphere. Effective population size and growth rate were negatively correlated with global surface temperatures, in line with global parameters driving long-term demographic trends. Zootoca vivipara's ancient demography was neither driven by a single clade, nor by the 2 clades that colonized huge geographic areas after the last glaciation. The low importance of local phenomena, suggests that the experimentally demonstrated high sensitivity of this species to short-term ecological changes is a response in order to cope with short-term and local changes. This suggests that what affected its long-term demographic trend the most, were not these local changes/responses, but rather the important and prolonged global climatic changes and important vegetation changes on the northern hemisphere, including the opening up of the forest by humans.

Effects of intrinsic environmental predictability on intra-individual and intra-population variability of plant reproductive traits and eco-evolutionary consequences.

BACKGROUND AND AIMS: It is widely accepted that changes in the environment affect mean trait expression, but little is known about how the environment shapes intra-individual and intra-population variance. Theory suggests that intra-individual variance might be plastic and under natural selection, rather than reflecting developmental noise, but evidence for this hypothesis is scarce. Here, we experimentally tested whether differences in intrinsic environmental predictability affect intra-individual and intra-population variability of different reproductive traits, and whether intra-individual variability is under selection. METHODS: Under field conditions, we subjected Onobrychis viciifolia to more and less predictable precipitation over 4 generations and 4 years. We analysed effects on the coefficient of intra-individual variation (CVi-i) and the coefficient of intra-population variation (CVi-p), assessed whether the coefficients of intra-individual variation (CsVi-i) are under natural selection and tested for transgenerational responses (ancestor environmental effects on offspring). KEY RESULTS: Less predictable precipitation led to higher CsVi-i and CsVi-p, consistent with plastic responses. The CsVi-i of all studied traits were under consistent stabilizing selection, and precipitation predictability affected the strength of selection and the location of the optimal CVi-i of a single trait. All CsVi-i differed from the optimal CVi-i and the maternal and offspring CsVi-i were positively correlated, showing that there was scope for change. Nevertheless, no consistent transgenerational effects were found in any of the three descendant generations, which contrasts with recent studies that detected rapid transgenerational responses in the trait means of different plant species. This suggests that changes in intra-individual variability take longer to evolve than changes in trait means, which may explain why high intra-individual variability is maintained, despite the stabilizing selection. CONCLUSIONS: The results indicate that plastic changes of intra-individual variability are an important determinant of whether plants will be able to cope with changes in environmental predictability induced by the currently observed climatic change.

Maternal effects and urbanization: Variation of yolk androgens and immunoglobulin in city and forest blackbirds.

Wildlife inhabiting urban environments exhibit drastic changes in morphology, physiology, and behavior. It has often been argued that these phenotypic responses could be the result of micro-evolutionary changes following the urbanization process. However, other mechanisms such as phenotypic plasticity, maternal effects, and developmental plasticity could be involved as well. To address maternal effects as potential mechanisms, we compared maternal hormone and antibody concentrations in eggs between city and forest populations of European blackbirds (Turdus merula), a widely distributed species for which previous research demonstrated differences in behavioral and physiological traits. We measured egg and yolk mass, yolk concentrations of androgens (androstenedione [A4], testosterone [T], 5α-dihydrotestosterone [5α-DHT], and immunoglobulins [IgY]) and related them to population, clutch size, laying order, embryo sex, and progress of breeding season. We show (a) earlier onset of laying in the city than forest population, but similar egg and clutch size; (b) higher overall yolk androgen concentrations in the forest than the city population (sex-dependent for T); (c) greater among-female variation of yolk T and 5α-DHT concentrations in the forest than city population, but similar within-clutch variation; (d) similar IgY concentrations with a seasonal decline in both populations; and (e) population-specific positive (city) or negative (forest) association of yolk A4 and T with IgY concentrations. Our results are consistent with the hypotheses that hormone-mediated maternal effects contribute to differences in behavioral and physiological traits between city and forest individuals and that yolk androgen and immunoglobulin levels can exhibit population-specific relationships rather than trade-off against each other.

Decreased Precipitation Predictability Negatively Affects Population Growth through Differences in Adult Survival.

Global climate change is leading to decreased climatic predictability. Theoretical work indicates that changes in the climate's intrinsic predictability will affect population dynamics and extinction, but experimental evidence is scarce. Here, we experimentally tested whether differences in intrinsic precipitation predictability affect population dynamics of the European common lizard (Zootoca vivipara) by simulating more predictable (MP) and less predictable (LP) precipitation in 12 seminatural populations over 3 years and measuring different vital rates. A seasonal age-structured matrix model was parametrized to assess treatment effects on vital rates and asymptotic population growth (λ). There was a nonsignificant trend for survival being higher in MP than in LP precipitation, and no differences existed in reproductive rates. Small nonsignificant survival differences in adults explained changes in λ, and survival differences among age classes were in line with predictions from cohort resonance. As a result, λ was significantly higher in MP than in LP precipitation. This experimentally shows that small effects have major consequences on λ, that forecasted decreases in precipitation predictability are likely to exacerbate the current rate of population decline and extinction, and that stage-structured matrix models are required to unravel the aftermath of climate change.

Reversals in complex traits uncovered as reticulation events: Lessons from the evolution of parity-mode, chromosome morphology, and maternal resource transfer.

Complex traits include, among many others, the evolution of eyes, wings, body forms, reproductive modes, human intelligence, social behavior, diseases, and chromosome morphology. Dollo's law states that the evolution of complex traits is irreversible. However, potential exceptions have been proposed. Here, we investigated whether reticulation, a simple and elegant means by which complex characters may be reacquired, could account for suggested reversals in the evolution of complex characters using two datasets with sufficient genetic coverage and a total of five potential reversals. Our analyses uncovered a potential reversal in the evolution of parity mode and a potential reversal in the evolution of placentotrophy of fish (Cyprinodontiformes) as reticulation events. Moreover, in a reptile that exhibits a potential reversal from viviparity to oviparity (Zootoca vivipara), reticulation provided the most parsimonious explanation for sex chromosome evolution. Therefore, three of the five studied potential reversals were unraveled as reticulation events. This constitutes the first evidence that accounting for reticulation can fundamentally influence the interpretation of the evolution of complex traits, that testing for reticulation is crucial for obtaining robust phylogenies, and that complex ancestral characters may be reacquired through hybridization with a lineage that still exhibits the trait. Hybridization, rather than reappearance of ancestral traits by means of small evolutionary steps, may thus account for suggested exceptions to Dollo's law. Consequently, ruling out reticulation is required to claim the evolutionary reversal of complex characters and potential exceptions to Dollo's rule.

Rapid and positive responses of plants to lower precipitation predictability.

Current climate change is characterized by an increase in weather variability, which includes altered means, variance and predictability of weather parameters, and which may affect an organism's ecology and evolution. Few studies have experimentally manipulated the variability of weather parameters, and very little is known about the effects of changes in the intrinsic predictability of weather parameters on living organisms. Here, we experimentally tested the effects of differences in intrinsic precipitation-predictability on two herbaceous plants (Onobrychis viciifolia and Papaver rhoeas). Lower precipitation-predictability led to phenological advance and to an increase in reproductive success, and population growth. Both species exhibited rapid transgenerational responses in phenology and fitness-related traits across four generations that mitigated most effects of precipitation-predictability on fitness proxies of ancestors. Transgenerational responses appeared to be the result of changes in phenotypic plasticity rather than local adaptation. They mainly existed with respect to conditions prevailing during early, but not during late growth, suggesting that responses to differences in predictability during late growth might be more difficult. The results show that lower short-term predictability of precipitation positively affected fitness, rapid transgenerational responses existed and different time scales of predictability (short-term, seasonal and transgenerational predictability) may affect organisms differently. This shows that the time scale of predictability should be considered in evolutionary and ecological theories, and in assessments of the consequences of climate change.

Corticosterone mediated mate choice affects female mating reluctance and reproductive success.

The study of stress-related hormones as mediators of sexual selection has traditionally focused on the effect of glucocorticoids on male quality and competing ability. However, environmental stressors are expected to affect both males and females, and the strength of sexual selection might be affected by changes in female mating decisions, a hypothesis that has rarely been tested. Here, we investigated whether female common lizard (Zootoca vivipara) mating behaviour and mating preferences are affected by different levels of administered corticosterone and conditioned by the familiarity of their partners, which is known to influence Z. vivipara social behaviour. To this end, two females, one corticosterone-treated and one control female, were simultaneously presented with an unfamiliar male and the following day with either a familiar or an unfamiliar male. Females treated with corticosterone (Cort) were more aggressive towards males and mated less. Furthermore, copulation probability in Cort females, but not in control females, increased with body size. On the second day, Cort females only mated with familiar partners. In contrast, male behaviour towards females was not affected by treatment and only bigger males successfully copulated with Cort females. This shows that corticosterone directly affected female mating behaviour and mating preferences, while male mating behaviour was unaffected by the female's level of corticosterone. Environmental and social stressors may affect reproductive strategies of females, the strength of sexual selection, and sexual conflict through their effects on female glucocorticoid levels, potentially in a wide range of species.

A multi-year experiment shows that lower precipitation predictability encourages plants' early life stages and enhances population viability.

Climate change is a key factor that may cause the extinction of species. The associated reduced weather predictability may alter the survival of plants, especially during their early life stages, when individuals are most fragile. While it is expected that extreme weather events will be highly detrimental for species, the effects of more subtle environmental changes have been little considered. In a four-year experiment on two herbaceous plants, Papaver rhoeas and Onobrychis viciifolia, we manipulated the predictability of precipitation by changing the temporal correlation of precipitation events while maintaining average precipitation constant, leading to more and less predictable treatments. We assessed the effect of predictability on plant viability in terms of seedling emergence, survival, seed production, and population growth rate. We found greater seedling emergence, survival, and population growth for plants experiencing lower intra-seasonal predictability, but more so during early compared to late life stages. Since predictability levels were maintained across four generations, we have also tested whether descendants exhibited transgenerational responses to previous predictability conditions. In P. rhoeas, descendants had increased the seedling emergence compared to ancestors under both treatments, but more so under lower precipitation predictability. However, higher predictability in the late treatment induced higher survival in descendants, showing that these conditions may benefit long-term survival. This experiment highlights the ability of some plants to rapidly exploit environmental resources and increase their survival under less predictable conditions, especially during early life stages. Therefore, this study provides relevant evidence of the survival capacity of some species under current and future short-term environmental alterations.

Molecular evidence for host-parasite co-speciation between lizards and Schellackia parasites.

Current and past parasite transmission may depend on the overlap of host distributions, potentially affecting parasite specificity and co-evolutionary processes. Nonetheless, parasite diversification may take place in sympatry when parasites are transmitted by vectors with low mobility. Here, we test the co-speciation hypothesis between lizard final hosts of the Family Lacertidae, and blood parasites of the genus Schellackia, which are potentially transmitted by haematophagous mites. The effects of current distributional overlap of host species on parasite specificity are also investigated. We sampled 27 localities on the Iberian Peninsula and three in northern Africa, and collected blood samples from 981 individual lizards of seven genera and 18 species. The overall prevalence of infection by parasites of the genus Schellackia was ∼35%. We detected 16 Schellackia haplotypes of the 18S rRNA gene, revealing that the genus Schellackia is more diverse than previously thought. Phylogenetic analyses showed that Schellackia haplotypes grouped into two main monophyletic clades, the first including those detected in host species endemic to the Mediterranean region and the second those detected in host genera Acanthodactylus, Zootoca and Takydromus. All but one of the Schellackia haplotypes exhibited a high degree of host specificity at the generic level and 78.5% of them exclusively infected single host species. Some host species within the genera Podarcis (six species) and Iberolacerta (two species) were infected by three non-specific haplotypes of Schellackia, suggesting that host switching might have positively influenced past diversification of the genus. However, the results supported the idea that current host switching is rare because there existed a significant positive correlation between the number of exclusive parasite haplotypes and the number of host species with current sympatric distribution. This result, together with significant support for host-parasite molecular co-speciation, suggests that parasites of the genus Schellackia co-evolved with their lizard hosts.

Climate Effects on Growth, Body Condition, and Survival Depend on the Genetic Characteristics of the Population.

Climatic change is expected to affect individual life histories and population dynamics, potentially increasing vulnerability to extinction. The importance of genetic diversity has been highlighted for adaptation and population persistence. However, whether responses of life-history traits to a given environmental condition depend on the genetic characteristics of a population remains elusive. Here we tested this hypothesis in the lizard Zootoca vivipara by simultaneously manipulating habitat humidity, a major climatic predictor of Zootoca's distribution, and adult male color morph frequency, a trait with genome-wide linkage. Interactive effects of humidity and morph frequency had immediate effects on growth and body condition of juveniles and yearlings, as well as on adult survival, and delayed effects on offspring size. In yearlings, higher humidity led to larger female body size and lower humidity led to higher male compared to female survival. In juveniles and yearlings, some treatment effects were compensated over time. The results show that individual responses to environmental conditions depend on the population's color morph frequency, age class, and sex and that these affect intra- and inter-age class competition. Moreover, humidity affected the competitive environment rather than imposing trait-based selection on specific color morphs. This indicates that species' responses to changing environments (e.g., to climate change) are highly complex and difficult to accurately reconstruct and predict without information on the genetic characteristics and demographic structure of populations.

Inter-class competition in stage-structured populations: effects of adult density on life-history traits of adult and juvenile common lizards.

Ecological and evolutionary processes in natural populations are largely influenced by the population's stage-structure. Commonly, different classes have different competitive abilities, e.g., due to differences in body size, suggesting that inter-class competition may be important and largely asymmetric. However, experimental evidence states that inter-class competition, which is important, is rare and restricted to marine fish. Here, we manipulated the adult density in six semi-natural populations of the European common lizard, Zootoca vivipara, while holding juvenile density constant. Adult density affected juveniles, but not adults, in line with inter-class competition. High adult density led to lower juvenile survival and growth before hibernation. In contrast, juvenile survival after hibernation was higher in populations with high adult density, pointing to relaxed inter-class competition. As a result, annual survival was not affected by adult density, showing that differences in pre- and post-hibernation survival balanced each other out. The intensity of inter-class competition affected reproduction, performance, and body size in juveniles. Path analyses unravelled direct treatment effects on early growth (pre-hibernation) and no direct treatment effects on the parameters measured after hibernation. This points to allometry of treatment-induced differences in early growth, and it suggests that inter-class competition mainly affects the early growth of the competitively inferior class and thereby their future performance and reproduction. These results are in contrast with previous findings and, together with results in marine fish, suggest that the strength and direction of density dependence may depend on the degree of inter-class competition, and thus on the availability of resources used by the competing classes.

Experimental evidence that sperm maturation drives protandry in an ectotherm.

Protandry, i.e., the earlier arrival to breeding areas of males than females, has attracted a lot of scientific attention. However, evidence for the evolutionary hypotheses of protandry is surprisingly scarce. Here, we experimentally manipulate the time of emergence from hibernation of males, relative to females, in the common lizard, Zootoca vivipara. We test whether the timing of emergence affects sperm maturation and mating success, to disentangle among proposed selective advantages of protandry. Our results experimentally demonstrate that the timing of emergence affects the date of sperm presence. Moreover, the degree of protandry affected whether males had sperm upon their first encounter with females, but it did not affect the probability of copulating. Mating occurred independent of male fertility and mating during infertility was least common in early emerging males. Early emergence from hibernation by males, relative to females, thus increases the male's chance of fertilising eggs and later emergence from hibernation by females reduces the female's probability of mating with infertile males. These results point to direct reproductive benefits of protandry in males and females, where earlier emergence is predicted to increase the male's opportunities to inseminate mates, and later emergence reduces the female's probability of copulating with infertile males. This suggests that protandry evolved due to the time required for sperm maturation after emergence from hibernation.

Microhabitat selection in the common lizard: implications of biotic interactions, age, sex, local processes, and model transferability among populations.

Modeling species' habitat requirements are crucial to assess impacts of global change, for conservation efforts and to test mechanisms driving species presence. While the influence of abiotic factors has been widely examined, the importance of biotic factors and biotic interactions, and the potential implications of local processes are not well understood. Testing their importance requires additional knowledge and analyses at local habitat scale. Here, we recorded the locations of species presence at the microhabitat scale and measured abiotic and biotic parameters in three different common lizard (Zootoca vivipara) populations using a standardized sampling protocol. Thereafter, space use models and cross-evaluations among populations were run to infer local processes and estimate the importance of biotic parameters, biotic interactions, sex, and age. Biotic parameters explained more variation than abiotic parameters, and intraspecific interactions significantly predicted the spatial distribution. Significant differences among populations in the relationship between abiotic parameters and lizard distribution, and the greater model transferability within populations than between populations are in line with effects predicted by local adaptation and/or phenotypic plasticity. These results underline the importance of including biotic parameters and biotic interactions in space use models at the population level. There were significant differences in space use between sexes, and between adults and yearlings, the latter showing no association with the measured parameters. Consequently, predictive habitat models at the population level taking into account different sexes and age classes are required to understand a specie's ecological requirements and to allow for precise conservation strategies. Our study therefore stresses that future predictive habitat models at the population level and their transferability should take these parameters into account.

Ecological change predicts population dynamics and genetic diversity over 120 000 years.

While ecological effects on short-term population dynamics are well understood, their effects over millennia are difficult to demonstrate and convincing evidence is scant. Using coalescent methods, we analysed past population dynamics of three lizard species (Psammodromus hispanicus, P. edwardsianus, P. occidentalis) and linked the results with climate change data covering the same temporal horizon (120 000 years). An increase in population size over time was observed in two species, and in P. occidentalis, no change was observed. Temporal changes in temperature seasonality and the maximum temperature of the warmest month were congruent with changes in population dynamics observed for the three species and both variables affected population density, either directly or indirectly (via a life-history trait). These results constitute the first solid link between ecological change and long-term population dynamics. The results moreover suggest that ecological change leaves genetic signatures that can be retrospectively traced, providing evidence that ecological change is a crucial driver of genetic diversity and speciation.

Geographical and temporal body size variation in a reptile: roles of sex, ecology, phylogeny and ecology structured in phylogeny.

Geographical body size variation has long interested evolutionary biologists, and a range of mechanisms have been proposed to explain the observed patterns. It is considered to be more puzzling in ectotherms than in endotherms, and integrative approaches are necessary for testing non-exclusive alternative mechanisms. Using lacertid lizards as a model, we adopted an integrative approach, testing different hypotheses for both sexes while incorporating temporal, spatial, and phylogenetic autocorrelation at the individual level. We used data on the Spanish Sand Racer species group from a field survey to disentangle different sources of body size variation through environmental and individual genetic data, while accounting for temporal and spatial autocorrelation. A variation partitioning method was applied to separate independent and shared components of ecology and phylogeny, and estimated their significance. Then, we fed-back our models by controlling for relevant independent components. The pattern was consistent with the geographical Bergmann's cline and the experimental temperature-size rule: adults were larger at lower temperatures (and/or higher elevations). This result was confirmed with additional multi-year independent data-set derived from the literature. Variation partitioning showed no sex differences in phylogenetic inertia but showed sex differences in the independent component of ecology; primarily due to growth differences. Interestingly, only after controlling for independent components did primary productivity also emerge as an important predictor explaining size variation in both sexes. This study highlights the importance of integrating individual-based genetic information, relevant ecological parameters, and temporal and spatial autocorrelation in sex-specific models to detect potentially important hidden effects. Our individual-based approach devoted to extract and control for independent components was useful to reveal hidden effects linked with alternative non-exclusive hypothesis, such as those of primary productivity. Also, including measurement date allowed disentangling and controlling for short-term temporal autocorrelation reflecting sex-specific growth plasticity.

Cumulative frequency-dependent selective episodes allow for rapid morph cycles and rock-paper-scissors dynamics in species with overlapping generations.

Rock-paper-scissors (RPS) dynamics, which maintain genetic polymorphisms over time through negative frequency-dependent (FD) selection, can evolve in short-lived species with no generational overlap, where they produce rapid morph frequency cycles. However, most species have overlapping generations and thus, rapid RPS dynamics are thought to require stronger FD selection, the existence of which yet needs to be proved. Here, we experimentally demonstrate that two cumulative selective episodes, FD sexual selection reinforced by FD selection on offspring survival, generate sufficiently strong selection to generate rapid morph frequency cycles in the European common lizard Zootoca vivipara, a multi-annual species with major generational overlap. These findings show that the conditions required for the evolution of RPS games are fulfilled by almost all species exhibiting genetic polymorphisms and suggest that RPS games may be responsible for the maintenance of genetic diversity in a wide range of species.

Multilocus phylogeography of the common lizard Zootoca vivipara at the Ibero-Pyrenean suture zone reveals lowland barriers and high-elevation introgression.

BACKGROUND: The geographic distribution of evolutionary lineages and the patterns of gene flow upon secondary contact provide insight into the process of divergence and speciation. We explore the evolutionary history of the common lizard Zootoca vivipara (= Lacerta vivipara) in the Iberian Peninsula and test the role of the Pyrenees and the Cantabrian Mountains in restricting gene flow and driving lineage isolation and divergence. We also assess patterns of introgression among lineages upon secondary contact, and test for the role of high-elevation trans-mountain colonisations in explaining spatial patterns of genetic diversity. We use mtDNA sequence data and genome-wide AFLP loci to reconstruct phylogenetic relationships among lineages, and measure genetic structure. RESULTS: The main genetic split in mtDNA corresponds generally to the French and Spanish sides of the Pyrenees as previously reported, in contrast to genome-wide AFLP data, which show a major division between NW Spain and the rest. Both types of markers support the existence of four distinct and geographically congruent genetic groups, which are consistent with major topographic barriers. Both datasets reveal the presence of three independent contact zones between lineages in the Pyrenean region, one in the Basque lowlands, one in the low-elevation mountains of the western Pyrenees, and one in the French side of the central Pyrenees. The latter shows genetic evidence of a recent, high-altitude trans-Pyrenean incursion from Spain into France. CONCLUSIONS: The distribution and age of major lineages is consistent with a Pleistocene origin and a role for both the Pyrenees and the Cantabrian Mountains in driving isolation and differentiation of Z. vivipara lineages at large geographic scales. However, mountain ranges are not always effective barriers to dispersal, and have not prevented a recent high-elevation trans-Pyrenean incursion that has led to asymmetrical introgression among divergent lineages. Cytonuclear discordance in patterns of genetic structure and introgression at contact zones suggests selection may be involved at various scales. Suture zones are important areas for the study of lineage formation and speciation, and our results show that biogeographic barriers can yield markedly different phylogeographic patterns in different vertebrate and invertebrate taxa.