| 1. |
- MacGregor, Hannah E A, et al.
(author)
-
Chemical communication, sexual selection, and introgression in wall lizards
- 2017
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In: Evolution. - : Wiley. - 0014-3820. ; 71:10, s. 2327-2343
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Journal article (peer-reviewed)abstract
- Divergence in communication systems should influence the likelihood that individuals from different lineages interbreed, and consequently shape the direction and rate of hybridization. Here, we studied the role of chemical communication in hybridization, and its contribution to asymmetric and sexually selected introgression between two lineages of the common wall lizard (Podarcis muralis). Males of the two lineages differed in the chemical composition of their femoral secretions. Chemical profiles provided information regarding male secondary sexual characters, but the associations were variable and inconsistent between lineages. In experimental contact zones, chemical composition was weakly associated with male reproductive success, and did not predict the likelihood of hybridization. Consistent with these results, introgression of chemical profiles in a natural hybrid zone resembled that of neutral nuclear genetic markers overall, but one compound in particular (tocopherol methyl ether) matched closely the introgression of visual sexual characters. These results imply that associations among male chemical profiles, sexual characters, and reproductive success largely reflect transient and environmentally driven effects, and that genetic divergence in chemical composition is largely neutral. We therefore suggest that femoral secretions in wall lizards primarily provide information about residency and individual identity rather than function as sexual signals.
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| 2. |
- Andrade, Pedro, et al.
(author)
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Regulatory changes in pterin and carotenoid genes underlie balanced color polymorphisms in the wall lizard
- 2019
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In: Proceedings of the National Academy of Sciences of the United States of America. - : Proceedings of the National Academy of Sciences. - 0027-8424 .- 1091-6490. ; 116:12, s. 5633-5642
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Journal article (peer-reviewed)abstract
- 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.
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| 3. |
- Botterill-James, Thomas, et al.
(author)
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Experimental manipulation suggests effect of polyandry but not mate familiarity on within-pair aggression in the social skink, Liopholis whitii
- 2017
-
In: Behavioral Ecology and Sociobiology. - : Springer Science and Business Media LLC. - 0340-5443 .- 1432-0762. ; 71:4
-
Journal article (peer-reviewed)abstract
- Abstract: Long-term monogamy is a key characteristic of family living across animals. The evolutionary maintenance of long-term monogamy has been suggested to be facilitated by increased reproductive coordination as a result of mate familiarity, leading to increased reproductive success. However, such effects can be compromised if females mate outside the pair bond (e.g. female polyandry), introducing conflicts of interest between the male and female. Here, we experimentally test the effects of both mate familiarity and female polyandry on agonistic behaviour and reproduction in a family living lizard, Liopholis whitii. We found that mate familiarity did not decrease the level of aggression between pairs whereas reducing female polyandry did. However, we did not find an effect of either mate familiarity or female polyandry on female reproductive output. These results suggest that male behavioural responses to female polyandry may influence pair stability in Liopholis whitii, providing support for the growing appreciation of the multiple ways in which female polyandry can influence the stability of family living. Significance statement: Family living is underpinned by social pair bonds between adults (i.e. stable social monogamy). Therefore, key to understanding the emergence and maintenance of family living is identifying factors influencing pair bonds. We manipulated both female polyandry and mate familiarly in replicated enclosure experiment using social lizards to test their role in mediating within-pair aggression and ultimately the coordination of reproductive behaviour and hence reproductive output. We found that polyandry but not mate familiarity influenced levels of aggression between pairs but this did not transmit into concomitant effects on reproductive output.
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| 4. |
- Botterill-James, Thomas, et al.
(author)
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Family aggression in a social lizard
- 2017
-
In: Scientific Reports. - : Springer Science and Business Media LLC. - 2045-2322. ; 7:1
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Journal article (peer-reviewed)abstract
- The evolution of family living is underpinned by conflict and cooperation between family members. While family groups can be maintained by reducing conflict between parents and offspring, interactions between siblings may play an equally important role. Here, we compared the level of aggressive interactions between siblings to that between parents and their offspring in the family living skink Liopholis whitii. Aggressive interactions occurred much more frequently between siblings and between fathers and offspring than between mothers and their offspring. These results suggest that ecological and social conditions that reduce conflict between siblings and between males and offspring will be fundamental in the evolutionary maintenance and diversification of family living in these lizards.
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| 5. |
- Bouffet-Halle, Alix, et al.
(author)
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Characterisation and cross-amplification of sex-specific genetic markers in Australasian Egerniinae lizards and their implications for understanding the evolution of sex determination and social complexity
- 2022
-
In: Australian Journal of Zoology. - 0004-959X. ; 69:2, s. 33-40
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Journal article (peer-reviewed)abstract
- Sex is a pervasive factor that underpins functional phenotypic variation across a range of traits. Although sex can usually be distinguished morphologically, in some species this is not possible. The development of genetic markers for sex identification is, thus, key if we are to incorporate sex into an understanding of ecological or evolutionary process. Here we develop genetic markers for the identification of sex within an iconic Australian lizard group, the Egernia group, which is notable for its complex social behaviour. We used restriction-site associated DNA sequencing to characterise sex-specific genetic sequences for a key member of the group, Liopholis whitii, and designed primers for four of these putative sex-specific sequences. These primers amplified across some, but not all, species of the group. Our results provided several important insights. They suggest conservatism of a XX/XY sex determination system within the group as well as sex-specific genomic regions that appear independent of the conserved genomic regions identified in other skink species. More broadly, the development of sex markers for the Egernia group opens up a range of potential research questions related to the role that sex plays in the mediation of social behaviour and, through this, the emergence and stability of social life.
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| 6. |
- Feiner, Nathalie, et al.
(author)
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Adaptive introgression reveals the genetic basis of a sexually selected syndrome in wall lizards
- 2024
-
In: Science Advances. - : American Association for the Advancement of Science (AAAS). - 2375-2548. ; 10:14
-
Journal article (peer-reviewed)abstract
- 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 similar to 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.
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| 7. |
- Feiner, Nathalie, et al.
(author)
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Developmental plasticity in reptiles: Insights from temperature-dependent gene expression in wall lizard embryos : Insights from temperature-dependent gene expression in wall lizard embryos
- 2018
-
In: Journal of experimental zoology. Part A, Ecological and integrative physiology. - : Wiley. - 2471-5638. ; 329:6-7, s. 351-361
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Journal article (peer-reviewed)abstract
- Many features of the development of reptiles are affected by temperature, but very little is known about how incubation temperature affects gene expression. Here, we provide a detailed case study of gene expression profiles in common wall lizard (Podarcis muralis) embryos developing at stressfully low (15°C) versus benign (24°C) temperature. For maximum comparability between the two temperature regimes, we selected a precise developmental stage early in embryogenesis defined by the number of somites. We used a split-clutch design and lizards from four different populations to evaluate the robustness of temperature-responsive gene expression profiles. Embryos incubated at stressfully low incubation temperature expressed on average 20% less total RNA than those incubated at benign temperatures, presumably reflecting lower rates of transcription at cool temperature. After normalizing for differences in total amounts of input RNA, we find that approximately 50% of all transcripts show significant expression differences between the two incubation temperatures. Transcripts with the most extreme changes in expression profiles are associated with transcriptional and translational regulation and chromatin remodeling, suggesting possible epigenetic mechanisms underlying acclimation of early embryos to cool temperature. We discuss our findings in light of current advances in the use of transcriptomic data to study how individuals acclimatize and populations adapt to thermal stress.
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| 8. |
- Feiner, Nathalie, et al.
(author)
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Signatures of selection in embryonic transcriptomes of lizards adapting in parallel to cool climate
- 2018
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In: Evolution. - : Wiley. - 0014-3820. ; 72:1, s. 67-81
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Journal article (peer-reviewed)abstract
- Populations adapting independently to the same environment provide important insights into the repeatability of evolution at different levels of biological organization. In the 20th century, common wall lizards (Podarcis muralis) from southern and western Europe were introduced to England, north of their native range. Nonnative populations of both lineages have adapted to the shorter season and lower egg incubation temperature by increasing the absolute rate of embryonic development. Here, we tested if this adaptation is accompanied by signatures of directional selection in the transcriptomes of early embryos and, if so, if nonnative populations show adaptive convergence. Embryos from nonnative populations exhibited gene expression profiles consistent with directional selection following introduction, but different genes were affected in the two lineages. Despite this, the functional enrichment of genes that changed their expression following introduction showed substantial similarity between lineages, and was consistent with mechanisms that should promote developmental rate. Moreover, the divergence between nonnative and native populations was enriched for genes that were temperature-responsive in native populations. These results indicate that small populations are able to adapt to new climatic regimes, but the means by which they do so may largely be determined by founder effects and other sources of genetic drift.
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| 9. |
- Halliwell, Ben, et al.
(author)
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Habitat saturation promotes delayed dispersal in a social reptile
- 2017
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In: Behavioral Ecology. - : Oxford University Press (OUP). - 1045-2249 .- 1465-7279. ; 28:2, s. 515-522
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Journal article (peer-reviewed)abstract
- When and where offspring disperse has important implications for the evolutionary emergence and maintenance of group living. In noncooperative breeders, direct benefits of delayed dispersal are relatively limited, suggesting that decisions regarding whether or not to remain in the parental territory are largely driven by the availability of suitable habitat in which to settle. Although there is ample evidence of correlations between habitat saturation and delayed dispersal, experimental tests are rare, particularly for species with facultative group formation. We manipulated the density of conspecifics in enclosed populations of a family living reptile to experimentally evaluate the influence of habitat saturation on the tendency to delay dispersal. Habitat saturation did not influence whether or not offspring explored their surroundings. However, when conspecific density was high, more offspring delayed dispersal and those that did settle in high-density enclosures had reduced survival. These patterns appear to be due to increased dispersal costs imposed by conspecific aggression; offspring that explored high-density enclosures had reduced body condition and a greater risk of mortality. We discuss these results in the context of the evolutionary origins of family living.
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| 10. |
- Halliwell, Ben, et al.
(author)
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Live bearing promotes the evolution of sociality in reptiles
- 2017
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In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 8:1
-
Journal article (peer-reviewed)abstract
- Identifying factors responsible for the emergence and evolution of social complexity is an outstanding challenge in evolutionary biology. Here we report results from a phylogenetic comparative analysis of over 1000 species of squamate reptile, nearly 100 of which exhibit facultative forms of group living, including prolonged parent–offspring associations. We show that the evolution of social groupings among adults and juveniles is overwhelmingly preceded by the evolution of live birth across multiple independent origins of both traits. Furthermore, the results suggest that live bearing has facilitated the emergence of social groups that remain stable across years, similar to forms of sociality observed in other vertebrates. These results suggest that live bearing has been a fundamentally important precursor in the evolutionary origins of group living in the squamates.
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| 11. |
- Hansson, Alexander, et al.
(author)
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Sex and early-life conditions shape telomere dynamics in an ectotherm
- 2024
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In: JOURNAL OF EXPERIMENTAL BIOLOGY. - 0022-0949 .- 1477-9145. ; 227:3
-
Journal article (peer-reviewed)abstract
- 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 longterm 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.
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| 12. |
- Heathcote, Robert J P, et al.
(author)
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Male behaviour drives assortative reproduction during the initial stage of secondary contact.
- 2016
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In: Journal of evolutionary biology. - : Wiley. - 1420-9101 .- 1010-061X. ; 29:5, s. 1003-1015
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Journal article (peer-reviewed)abstract
- Phenotypic divergence in allopatry can facilitate speciation by reducing the likelihood that individuals of different lineages hybridise during secondary contact. However, few studies have established the causes of reproductive isolation in the crucial early stages of secondary contact. Here we establish behavioural causes of assortative reproduction between two phenotypically divergent lineages of the European wall lizard (Podarcis muralis), which have recently come into secondary contact. Parentage was highly assortative in experimental contact zones. However, despite pronounced divergence in male phenotypes, including chemical and visual sexual signals, there was no evidence that females discriminated between males of the two lineages in staged interactions or under naturalistic free-ranging conditions. Instead, assortative reproduction was driven by male mate preferences and, to a lesser extent, male-male competition. The effects were more pronounced when the habitat structure promoted high lizard densities. These results emphasize that assortative reproduction can occur in the absence of female choice, and that male behaviour may play an important role in limiting hybridisation during the initial stages of secondary contact. This article is protected by copyright. All rights reserved.
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| 13. |
- Heathcote, Robert J. P., et al.
(author)
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The scent of sun worship: basking experience alters scent mark composition in male lizards
- 2014
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In: Behavioral Ecology and Sociobiology. - : Springer Science and Business Media LLC. - 1432-0762 .- 0340-5443. ; 68:5, s. 861-870
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Journal article (peer-reviewed)abstract
- Signals used in female choice should honestly advertise the benefits that males can provide, with direct benefits often argued as being more important than indirect benefits. However, the nature of direct benefits in species without paternal care or nuptial gifts is poorly understood. Previous studies on lizards suggest that females decide where to settle and assumedly who to mate with based on information contained in scent marks from territorial males. Access to high-quality thermal resources is crucial for female reproductive success. Females may therefore be able to detect and exploit thermal-induced variation in the chemical composition of male scent marks when assessing the quality of his territory. We show that the amount of time male wall lizards (Podarcis muralis) are allowed to bask significantly alters the chemical composition of their femoral secretions used in scent marking. The direction of the change is consistent with adaptive plasticity to maintain signalling efficacy under warm conditions that increase evaporation of femoral secretions. The compounds affected by basking experience included those previously associated with male quality or shown to mediate male-male competition in lizards. However, whilst female lizards could discriminate between scent marks of males that had experienced different basking conditions, they did not preferentially associate with the scent from males from high-quality thermal conditions. These results highlight the potential importance of a previously neglected environmental effect on chemical signalling. We suggest thermal effects may have significant consequences for scent-mark composition in variable environments, with potential repercussions on olfactory communication in lizards.
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| 14. |
- MacGregor, Hannah E A, et al.
(author)
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Comparison of reproductive investment in native and non-native populations of common wall lizards reveals sex differences in adaptive potential
- 2017
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In: Oikos. - : Wiley. - 0030-1299. ; 126:11, s. 1564-1574
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Journal article (peer-reviewed)abstract
- Non-native animals can encounter very different environments than those they are adapted to. Functional changes in morphology, physiology and life-history following introduction show that organisms can adapt both fast and efficiently. It remains unclear, however, if female reproductive characters and male sexually selected behaviour show the same adaptive potential. Furthermore, the invasion success and evolutionary trajectory of non-native species might often depend on the ability of the sexes to coordinate shifts in characters associated with reproductive strategy. The common wall lizard, Podarcis muralis, has been repeatedly introduced from southern Europe to England over the past 80 years. Lizards in England experience a cool, seasonal climate that effectively restricts recruitment to the first clutch of the season, whereas in their native range up to three clutches per season recruit. As a consequence, both females and males in non-native populations should benefit from reducing or even eliminating their reproductive investment in second clutches. Using a combination of field data and experiments, we show that non-native females produce relatively larger and heavier first seasonal clutches and smaller and lighter second seasonal clutches compared to native females. In contrast, non-native and native males do not differ in their territorial and sexual behaviour later in the season. An adaptive shift in male seasonal reproductive investment may be constrained because males use breeding females as cues for sexual behaviour. If this is so, we expect a general pattern across climatic regimes whereby female reproductive investment evolves first, with responses in males lagging behind.
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| 15. |
- MacGregor, Hannah E A, et al.
(author)
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Experimental contact zones reveal causes and targets of sexual selection in hybridizing lizards
- 2017
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In: Functional Ecology. - : Wiley. - 0269-8463 .- 1365-2435. ; 31:3, s. 742-752
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Journal article (peer-reviewed)abstract
- Divergence in sexually selected traits in allopatry should affect the degree and direction of hybridization. However, few studies have established the causes and targets of sexual selection during secondary contact. Common wall lizards (Podarcis muralis) from north-central Italy have highly exaggerated male sexual traits compared to populations in Western Europe. Using experimental populations, we show that this creates asymmetries in male dominance, spatial habitat use and reproductive success upon secondary contact. Hybridization occurred almost exclusively between males of the Italian lineage and females of the Western European lineage. We provide evidence to suggest stronger ongoing selection on male sexual traits within the dominant Italian lineage. However, these same characters did not predict hybridization, and hybrid matings contributed little to variance in male reproductive success. Instead, most hybrid offspring were sired by Italian males displaying phenotypes associated with lower within-lineage reproductive success. Thus, highly directional hybridization arises because some Italian males are out-competed within their own lineage but remain competitive relative to males of the other lineage. This pattern of hybridization is consistent with the direction of introgression in natural contact zones, but our data suggest that sexual selection acting through hybridization may be weak at the leading edge of natural hybrid zones.
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| 16. |
- MacLeod, Kirsty J., et al.
(author)
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Viviparous mothers impose stronger glucocorticoid-mediated maternal stress effects on their offspring than oviparous mothers
- 2021
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 11:23, s. 17238-17259
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Journal article (peer-reviewed)abstract
- 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.
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| 17. |
- Michaelides, Sozos N., et al.
(author)
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Loss of genetic diversity and increased embryonic mortality in non-native lizard populations
- 2016
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In: Molecular Ecology. - : Wiley. - 0962-1083. ; 25:17, s. 4113-4125
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Journal article (peer-reviewed)abstract
- 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.
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| 18. |
- Michaelides, Sozos N., et al.
(author)
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Widespread primary, but geographically restricted secondary, human introductions of wall lizards, Podarcis muralis
- 2015
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In: Molecular Ecology. - : Wiley. - 0962-1083. ; 24:11, s. 2702-2714
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Journal article (peer-reviewed)abstract
- Establishing the introduction pathways of alien species is a fundamental task in invasion biology. The common wall lizard, Podarcis muralis, has been widely introduced outside of its native range in both Europe and North America, primarily through escaped pets or deliberate release of animals from captive or wild populations. Here, we use Bayesian clustering, approximate Bayesian computation (ABC) methods and network analyses to reconstruct the origin and colonization history of 23 non-native populations of wall lizards in England. Our analyses show that established populations in southern England originate from at least nine separate sources of animals from native populations in France and Italy. Secondary introductions from previously established non-native populations were supported for eleven (47%) populations. In contrast to the primary introductions, secondary introductions were highly restricted geographically and appear to have occurred within a limited time frame rather than being increasingly common. Together, these data suggest that extant wall lizard populations in England are the result of isolated accidental and deliberate releases of imported animals since the 1970s, with only local translocation of animals from established non-native populations. Given that populations introduced as recently as 25years ago show evidence of having adapted to cool climate, discouraging further translocations may be important to prevent more extensive establishment on the south coast of England.
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| 19. |
- Michaelides, Sozos, et al.
(author)
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Phylogeography and conservation genetics of the common wall lizard, Podarcis muralis, on islands at its northern range.
- 2015
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In: PLoS ONE. - : Public Library of Science (PLoS). - 1932-6203. ; 10:2
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Journal article (peer-reviewed)abstract
- Populations at range limits are often characterized by lower genetic diversity, increased genetic isolation and differentiation relative to populations at the core of geographical ranges. Furthermore, it is increasingly recognized that populations situated at range limits might be the result of human introductions rather than natural dispersal. It is therefore important to document the origin and genetic diversity of marginal populations to establish conservation priorities. In this study, we investigate the phylogeography and genetic structure of peripheral populations of the common European wall lizard, Podarcis muralis, on Jersey (Channel Islands, UK) and in the Chausey archipelago. We sequenced a fragment of the mitochondrial cytochrome b gene in 200 individuals of P. muralis to infer the phylogeography of the island populations using Bayesian approaches. We also genotyped 484 individuals from 21 populations at 10 polymorphic microsatellite loci to evaluate the genetic structure and diversity of island and mainland (Western France) populations. We detected four unique haplotypes in the island populations that formed a sub-clade within the Western France clade. There was a significant reduction in genetic diversity (HO, HE and AR) of the island populations in relation to the mainland. The small fragmented island populations at the northern range margin of the common wall lizard distribution are most likely native, with genetic differentiation reflecting isolation following sea level increase approximately 7000 BP. Genetic diversity is lower on islands than in marginal populations on the mainland, potentially as a result of early founder effects or long-term isolation. The combination of restriction to specific localities and an inability to expand their range into adjacent suitable locations might make the island populations more vulnerable to extinction.
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| 20. |
- Miñano, Maravillas Ruiz, et al.
(author)
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Climate shapes the geographic distribution and introgressive spread of color ornamentation in common wall lizards
- 2021
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In: American Naturalist. - : University of Chicago Press. - 0003-0147 .- 1537-5323. ; 198:3, s. 379-393
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Journal article (peer-reviewed)abstract
- Climate 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.
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| 21. |
- Noble, Daniel W.A., et al.
(author)
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Data Descriptor : A comprehensive database of thermal developmental plasticity in reptiles
- 2018
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In: Scientific Data. - : Springer Science and Business Media LLC. - 2052-4463. ; 5
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Journal article (peer-reviewed)abstract
- How temperature influences development has direct relevance to ascertaining the impact of climate change on natural populations. Reptiles have served as empirical models for understanding how the environment experienced by embryos can influence phenotypic variation, including sex ratio, phenology and survival. Such an understanding has important implications for basic eco-evolutionary theory and conservation efforts worldwide. While there is a burgeoning empirical literature of experimental manipulations of embryonic thermal environments, addressing widespread patterns at a comparative level has been hampered by the lack of accessible data in a format that is amendable to updates as new studies emerge. Here, we describe a database with nearly 10, 000 phenotypic estimates from 155 species of reptile, collected from 300 studies manipulating incubation temperature (published between 1974-2016). The data encompass various morphological, physiological, behavioural and performance traits along with growth rates, developmental timing, sex ratio and survival (e.g., hatching success). This resource will serve as an important data repository for addressing overarching questions about thermal plasticity of reptile embryos.
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| 22. |
- Paredes, Ursula, et al.
(author)
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Low Incubation Temperature Induces DNA Hypomethylation in Lizard Brains
- 2016
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In: Journal of Experimental Zoology Part A: Ecological Genetics and Physiology. - : Wiley. - 1932-5223. ; 325:6, s. 390-395
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Journal article (peer-reviewed)abstract
- Developmental stress can have organizational effects on suites of physiological, morphological, and behavioral characteristics. In lizards, incubation temperature is perhaps the most significant environmental variable affecting embryonic development. Wall lizards (Podarcis muralis) recently introduced by humans from Italy to England experience stressfully cool incubation conditions, which we here show reduce growth and increase the incidence of scale malformations. Using a methylation-sensitive AFLP protocol optimized for vertebrates, we demonstrate that this low incubation temperature also causes hypomethylation of DNA in brain tissue. A consistent pattern across methylation-susceptible AFLP loci suggests that hypomethylation is a general response and not limited to certain CpG sites. The functional consequences of hypomethylation are unknown, but it could contribute to genome stability and regulation of gene expression. Further studies of the effects of incubation temperature on DNA methylation in ectotherm vertebrates may reveal mechanisms that explain why the embryonic thermal environment often has physiological and behavioral consequences for offspring.
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| 23. |
- Pettersen, Amanda K., et al.
(author)
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How do fluctuating temperatures alter the cost of development?
- 2024
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In: Functional Ecology. - 0269-8463. ; , s. 114-125
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Journal article (peer-reviewed)abstract
- Quantifying how variable temperature regimes affect energy expenditure during development is crucial for understanding how future thermal regimes may impact early life survival and population persistence. Developmental cost theory (DCT) suggests that there is an optimal temperature (Topt) that minimises energy expenditure during development (the ‘cost of development‘). Exposure to fluctuating temperatures around an average of Topt is anticipated to increase either development time or metabolic rate. As a result, embryos will rapidly deplete yolk reserves, and consequently hatch at a smaller size or with less residual yolk to support postnatal survival and growth. Here, we studied total embryonic energy expenditure (development time and rate of CO2 production) and conversion of yolk into tissue in common wall lizards (Podarcis muralis) under three incubation treatments anticipated, based on DCT, to increase the cost of development: no variance (Topt constant, 24°C), low variance (22°C–26°C) and high variance (18°C–30°C). As predicted, we found that increasing variance around Topt increased the cost of development, despite reducing time to hatching. As a consequence, embryos on average hatched with 59% lower residual yolk reserves under high variance versus the constant incubation temperature treatment. Our results highlight how the relative temperature sensitivities of development time and metabolic rate determine the cost of development, which in turn may predict the ability of egg-laying ectotherms to persist in variable environments. We show that DCT can provide a mechanistic framework for understanding the widespread, but often seemingly idiosyncratic, effects of fluctuating incubation temperatures on hatchling tissue and residual yolk mass. Read the free Plain Language Summary for this article on the Journal blog.
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| 24. |
- Rago, Alfredo, et al.
(author)
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Introduction pathway and climate trump ecology and life history as predictors of establishment success in alien amphibians
- 2012
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 2:7, s. 1437-1445
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Journal article (peer-reviewed)abstract
- A major goal for ecology and evolution is to understand how abiotic and biotic factors shape patterns of biological diversity. Here, we show that variation in establishment success of nonnative frogs and toads is primarily explained by variation in introduction pathways and climatic similarity between the native range and introduction locality, with minor contributions from phylogeny, species ecology, and life history. This finding contrasts with recent evidence that particular species characteristics promote evolutionary range expansion and reduce the probability of extinction in native populations of amphibians, emphasizing how different mechanisms may shape species distributions on different temporal and spatial scales. We suggest that contemporary changes in the distribution of amphibians will be primarily determined by human-mediated extinctions and movement of species within climatic envelopes, and less by species-typical traits.
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| 25. |
- Ruiz Miñano, Maravillas, et al.
(author)
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Population genetic differentiation and genomic signatures of adaptation to climate in an abundant lizard
- 2022
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In: Heredity. - : Springer Science and Business Media LLC. - 0018-067X .- 1365-2540. ; 128:4, s. 271-278
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Journal article (peer-reviewed)abstract
- 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.
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| 26. |
- Uller, Tobias, et al.
(author)
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Genetic differentiation predicts body size divergence between island and mainland populations of common wall lizards (Podarcis muralis)
- 2019
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In: Biological Journal of the Linnean Society. - : Oxford University Press (OUP). - 0024-4066 .- 1095-8312. ; 127:4, s. 771-786
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Journal article (peer-reviewed)abstract
- Small-bodied vertebrates sometimes evolve gigantism on islands, but there is a lack of consistent association with ecological factors or island characteristics. One possible reason is that, even if the ecological conditions are right, body size might fail to diverge on islands that were isolated recently or if there is gene flow between islands and the mainland. We studied body size, ventral colour polymorphism and genetic structure across nine islands and adjacent mainland populations of common wall lizards (Podarcis muralis) off the western coast of France. Population genetic data suggested that island populations might have maintained gene flow after their geographical isolation from the mainland. Island lizards were larger and heavier than mainland lizards on average, but the extent of gigantism varied substantially between islands. Island size and distance from the mainland were poor predictors of body size, but lizards from populations that were highly genetically differentiated from the mainland were larger than lizards from less differentiated populations. Colour morphs that were rare on the mainland tended to be more common on islands. We propose that genetic isolation or bottlenecks promote body size evolution in island lizards, which makes it challenging to identify ecological causes of island gigantism without complementary genetic information.
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| 27. |
- While, Geoffrey M, et al.
(author)
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Adaptive responses to cool climate promotes persistence of a non-native lizard.
- 2015
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In: Royal Society of London. Proceedings B. Biological Sciences. - : The Royal Society. - 1471-2954. ; 282:1803
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Journal article (peer-reviewed)abstract
- 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.
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| 28. |
- While, Geoffrey M., et al.
(author)
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Egernia lizards
- 2015
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In: Current Biology. - : Elsevier BV. - 1879-0445 .- 0960-9822. ; 25:14, s. 593-595
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Journal article (other academic/artistic)
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| 29. |
- While, Geoffrey M, et al.
(author)
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Female reproductive investment in response to male phenotype in wall lizards and its implications for introgression
- 2017
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In: Biological Journal of the Linnean Society. - : Oxford University Press (OUP). - 0024-4066 .- 1095-8312. ; 121:4, s. 876-882
-
Journal article (peer-reviewed)abstract
- The likelihood that females will breed or how much they invest in reproduction can depend on the characters of their male partners. Such differential allocation may enhance or limit gene flow between hybridizing lineages, in particular when the lineages have diverged in sexually selected characters. Populations of the common wall lizard (Podarcis muralis) in some regions of Italy exhibit striking exaggeration of coloration, morphology and behaviour compared to populations in France. The two forms hybridize in north-western Italy. Gene flow is directional and in concordance with the prediction that the exaggerated sexual characters of lizards of Italian origin give them a mating advantage. To evaluate if differential allocation contributes to asymmetric introgression, we tested experimentally if female reproductive investment is affected by male origin and male secondary sexual characters. Despite the large genetic and phenotypic divergence between males of Italian and French origin, females did not invest more when paired with males of the same origin, nor when paired with males with highly expressed sexual characters. Combined, these results suggest that female responses to male phenotypes in wall lizards are unimportant for explaining the directional pattern of gene flow in regions of secondary contact.
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| 30. |
- While, Geoffrey M., et al.
(author)
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Patterns of developmental plasticity in response to incubation temperature in reptiles
- 2018
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In: Journal of Experimental Zoology Part A: Ecological and Integrative Physiology. - : Wiley. - 2471-5638 .- 2471-5646. ; 329:4-5, s. 162-176
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Journal article (peer-reviewed)abstract
- Early life environments shape phenotypic development in important ways that can lead to long-lasting effects on phenotype and fitness. In reptiles, one aspect of the early environment that impacts development is temperature (termed 'thermal developmental plasticity'). Indeed, the thermal environment during incubation is known to influence morphological, physiological, and behavioral traits, some of which have important consequences for many ecological and evolutionary processes. Despite this, few studies have attempted to synthesize and collate data from this expansive and important body of research. Here, we systematically review research into thermal developmental plasticity across reptiles, structured around the key papers and findings that have shaped the field over the past 50 years. From these papers, we introduce a large database (the 'Reptile Development Database') consisting of 9,773 trait means across 300 studies examining thermal developmental plasticity. This dataset encompasses data on a range of phenotypes, including morphological, physiological, behavioral, and performance traits along with growth rate, incubation duration, sex ratio, and survival (e.g., hatching success) across all major reptile clades. Finally, from our literature synthesis and data exploration, we identify key research themes associated with thermal developmental plasticity, important gaps in empirical research, and demonstrate how future progress can be made through targeted empirical, meta-analytic, and comparative work.
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| 31. |
- While, Geoffrey M., et al.
(author)
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Quo vadis amphibia? Global warming and breeding phenology in frogs, toads and salamanders
- 2014
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In: Ecography. - : Wiley. - 1600-0587 .- 0906-7590. ; 37:10, s. 921-929
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Journal article (peer-reviewed)abstract
- As the earth is getting warmer, many animals and plants have shifted their timing of breeding towards earlier dates. However, there is substantial variation between populations in phenological shifts that typically goes unexplained. Identification of the different location and species characteristics that drive such variable responses to global warming is crucial if we are to make predictions for how projected climate change scenarios will play out on local and global scales. Here we conducted a phylogenetically controlled meta-analysis of breeding phenology across frogs, toads and salamanders to examine the extent of variation in amphibian breeding phenology in response to global climate change. We show that there is strong geographic variation in response to global climate change, with species at higher latitudes exhibiting a more pronounced shift to earlier breeding than those at lower latitudes. Our analyses suggest that this latitude effect is a result of both the increased temperature (but not precipitation) at higher latitudes as well as a greater responsiveness by northern populations of amphibians to this change in temperature. We suggest that these effects should reinforce any direct effect of increasing warming at higher latitudes on breeding phenology. In contrast, we found very little contribution from other location factors or species traits. There was no evidence for a phylogenetic signal on advancing breeding phenology or responsiveness to temperature, suggesting that the amphibians that have been studied to date respond similarly to global warming.
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| 32. |
- While, Geoffrey M, et al.
(author)
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Sexual selection drives asymmetric introgression in wall lizards.
- 2015
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In: Ecology Letters. - : Wiley. - 1461-023X. ; 18:12, s. 1366-1375
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Journal article (other academic/artistic)abstract
- 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.
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| 33. |
- Yang, Weizhao, et al.
(author)
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Extensive introgression and mosaic genomes of Mediterranean endemic lizards
- 2021
-
In: Nature Communications. - : Springer Science and Business Media LLC. - 2041-1723. ; 12:1
-
Journal article (peer-reviewed)abstract
- 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.
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| 34. |
- Yang, Weizhao, et al.
(author)
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Genomic evidence for asymmetric introgression by sexual selection in the common wall lizard
- 2018
-
In: Molecular Ecology. - : Wiley. - 0962-1083.
-
Journal article (peer-reviewed)abstract
- 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.
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| 35. |
- Yang, Weizhao, et al.
(author)
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Population Genomics of Wall Lizards Reflects the Dynamic History of the Mediterranean Basin
- 2022
-
In: Molecular biology and evolution. - : Oxford University Press (OUP). - 0737-4038 .- 1537-1719. ; 39:1
-
Journal article (peer-reviewed)abstract
- 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.
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| 36. |
- Yang, Weizhao, et al.
(author)
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Spatial variation in gene flow across a hybrid zone reveals causes of reproductive isolation and asymmetric introgression in wall lizards
- 2020
-
In: Evolution. - : Wiley. - 0014-3820 .- 1558-5646. ; 74:7, s. 1289-1300
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Journal article (peer-reviewed)abstract
- 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.
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