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

Miñano, Maravillas Ruiz; While, Geoffrey M.; Yang, Weizhao; Burridge, Christopher P.; Salvi, Daniele; Uller, Tobias

doi:10.1038/s41437-022-00518-0

Cited by 14 publications

(10 citation statements)

References 76 publications

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“…For example, the long‐term geographic isolation and climatic heterogeneity in southwestern China might have shaped genetic diversification and promoted local adaptation of the evergreen oak Quercus kerrii (Jiang et al, 2018). Similarly, a previous study revealed that climatic variability had played a major role in shaping population genetic differentiation of the lizard Podarcis muralis in central Italy (Minano et al, 2022). In this study, we found distinct climate differences between habitats of European and Chinese D. galeata populations based on 19 climate variables: European populations inhabited a “cold and dry” climate whereas Chinese populations inhabited a “hot and wet” climate.…”

Section: Discussionmentioning

confidence: 71%

“…For example, the long-term geographic isolation and climatic heterogeneity in southwestern China might have shaped genetic diversification and promoted local adaptation of the evergreen oak Quercus kerrii (Jiang et al, 2018). Similarly, a previous study revealed that climatic variability had played a major role in shaping population genetic differentiation of the lizard Podarcis muralis in central Italy (Minano et al, 2022) We identified 4568 SNPs in D. galeata that were significantly associated with climatic PC1, which mainly reflects variation in annual mean temperature. Some genes linked to these SNPs have been previously implicated in climate adaptation, such as the ecdysone signalling gene dib and sad (Ma, Li, et al, 2019) and the stress response gene HSP90B1 (Sandoval-Castillo et al, 2020).…”

Section: Morphological Variabilitymentioning

confidence: 68%

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Climate has contributed to population diversification of Daphnia galeata across Eurasia

Deng,

Zhang,

Wolinska

et al. 2023

Molecular Ecology

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Climate is a fundamental abiotic factor that plays a key role in driving the evolution, distribution and population diversification of species. However, there have been few investigations of genomic signatures of adaptation to local climatic conditions in cladocerans. Here, we have provided the first high‐quality chromosome‐level genome assembly (~143 Mb, scaffold N50 12.6 Mb) of the waterflea, Daphnia galeata, and investigated genomic variation in 22 populations from Central Europe and Eastern China. Our ecological‐niche models suggested that the historic distribution of D. galeata in Eurasia was significantly affected by Quaternary climate fluctuations. We detected pronounced genomic and morphometric divergences between European and Chinese D. galeata populations. Such divergences could be partly explained by genomic signatures of thermal adaptation to distinct climate regimes: a set of candidate single‐nucleotide polymorphisms (SNPs) potentially associated with climate were detected. These SNPs were in genes significantly enriched in the Gene ontology terms “determination of adult lifespan” and “translation repressor activity”, and especially, mthl5 and SOD1 involved in the IIS pathway, and EIF4EBP2 involved in the target of the rapamycin signalling pathway. Our study indicates that certain alleles might be associated with particular temperature regimes, playing a functional role in shaping the population structure of D. galeata at a large geographical scale. These results highlight the potential role of molecular variation in the response to climate variation, in the context of global climate change.

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Section: Discussionmentioning

confidence: 71%

Section: Morphological Variabilitymentioning

confidence: 68%

Climate has contributed to population diversification of Daphnia galeata across Eurasia

Deng,

Zhang,

Wolinska

et al. 2023

Molecular Ecology

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“…However, our results did not reveal isolated lines, but almost null or very shallow divergence amongst P. muralis populations within the mtDNA clades in this area. Yet, the use of nuclear markers ( Psonis et al 2018 , Yang et al 2020 , Yang et al 2022 , Ruiz-Miñano et al 2022 ) is needed for assessing more detailed patterns of variation.…”

Section: Discussionmentioning

confidence: 99%

Unravelling the origin of the common wall lizards (Podarcis muralis) in outh-eastern Europe using mitochondrial evidence

Oskyrko¹,

Sos²,

Vacheva³

et al. 2022

BDJ

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The origin of the common wall lizards (Podarcis muralis) populations in south-eastern Europe (namely in Bulgaria and Romania), representing the north-eastern range border of this species, was addressed using mitochondrial DNA. We compared cytochrome b sequences from Bulgaria and Romania with those from the contiguous range in Central Europe that are available from previous studies. We recorded five main haplogroups in Bulgaria and Romania, belonging to the Central Balkan clade. However, haplogroup III was recorded in more localities than previously found. Additionally, signs of haplotype admixture were identified in several populations along the Danube River. The presence of the Southern Alps haplotype in one population from Otopeni, Bucharest (Romania) and its close phylogenetic relationships to north Italy populations suggests human-mediated introductions of this wall lizard clade in Romania. Our results confirm that P. muralis can have non-native lineages and admixture through active human-mediated transport.

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“…Here, we study population divergence in maternal investment, and embryo energy use and allocation across a climatic gradient in the widespread common wall lizard Podarcis muralis (Figure 1a) from the western Italian coast eastward into the Apennine mountains in central Italy. Wall lizards are abundant across this region, which spans >800 m in altitude and represent a transition in climatic regime from warm (low altitude) to cool (high altitude) climate (Ruiz Miñano et al, 2022). There is likely no single mechanism acting to compensate for the greater energy cost associated with embryonic development in cool climates, but rather a suite of complementary mechanisms.…”

Section: Introductionmentioning

confidence: 99%

Population divergence in maternal investment and embryo energy use and allocation suggests adaptive responses to cool climates

Pettersen

Ruuskanen

Nord

et al. 2023

Journal of Animal Ecology

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The thermal sensitivity of early life stages can play a fundamental role in constraining species distributions. For egg‐laying ectotherms, cool temperatures often extend development time and exacerbate developmental energy cost. Despite these costs, egg laying is still observed at high latitudes and altitudes. How embryos overcome the developmental constraints posed by cool climates is crucial knowledge for explaining the persistence of oviparous species in such environments and for understanding thermal adaptation more broadly. Here, we studied maternal investment and embryo energy use and allocation in wall lizards spanning altitudinal regions, as potential mechanisms that enable successful development to hatching in cool climates. Specifically, we compared population‐level differences in (1) investment from mothers (egg mass, embryo retention and thyroid yolk hormone concentration), (2) embryo energy expenditure during development, and (3) embryo energy allocation from yolk towards tissue. We found evidence that energy expenditure was greater under cool compared with warm incubation temperatures. Females from relatively cool regions did not compensate for this energetic cost of development by producing larger eggs or increasing thyroid hormone concentration in yolk. Instead, embryos from the high‐altitude region used less energy to complete development, that is, they developed faster without a concomitant increase in metabolic rate, compared with those from the low‐altitude region. Embryos from high altitudes also allocated relatively more energy towards tissue production, hatching with lower residual yolk: tissue ratios than low‐altitude region embryos. These results are consistent with local adaptation to cool climate and suggest that this is underpinned by mechanisms that regulate embryonic utilisation of yolk reserves and its allocation towards tissue, rather than shifts in maternal investment of yolk content or composition.

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

Cited by 14 publications

References 76 publications

Climate has contributed to population diversification of Daphnia galeata across Eurasia

Climate has contributed to population diversification of Daphnia galeata across Eurasia

Unravelling the origin of the common wall lizards (Podarcis muralis) in outh-eastern Europe using mitochondrial evidence

Population divergence in maternal investment and embryo energy use and allocation suggests adaptive responses to cool climates

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