Predator–prey interaction is a major force driving natural selection. Yet, the identification of species preying on, or consuming, aposematic species is largely unknown. Here, I conduct a study ...evaluating the role of the exotic Rattus rattus as a consumer and possible predator of the aposematic and toxic Salamandra salamandra. I used camera traps to investigate the response of R. rattus towards S. salamandra carcasses in two insular populations, Ons and San Martiño (NW Spain), which show remarkable contrasting behaviour (nocturnal vs. diurnal activity) and demographic and phenotypic differences. This study unveils R. rattus consumes S. salamandra despite its aposematic colour pattern and toxicity. The high number of salamander carcasses consumed or taken by rats throughout each island (90%–100%) and the lack of other possible predator–prey interactions points to R. rattus as an efficient consumer of S. salamandra in these insular environments, which might exert a high predation pressure on both islands. Yet, the drivers underlying the behavioural and phenotypic differences in these insular populations should be further investigated.
Predator–prey interaction is a major force driving natural selection. Rattus rattus consume aposematic and toxic Salamandra salamandra in two insular populations (NW Spain). Rattus rattus seems to exert a high predation pressure on S. salamandra, particularly on the small and diurnal population of San Martiño island.
Evolutionary changes in reproductive mode may affect co‐evolving traits, such as dispersal, although this subject remains largely underexplored. The shift from aquatic oviparous or larviparous ...reproduction to terrestrial viviparous reproduction in some amphibians entails skipping the aquatic larval stage and, thus, greater independence from water. Accordingly, amphibians exhibiting terrestrial viviparous reproduction may potentially disperse across a wider variety of suboptimal habitats and increase population connectivity in fragmented landscapes compared to aquatic‐breeding species. We investigated this hypothesis in the fire salamander (Salamandra salamandra), which exhibits both aquatic‐ (larviparity) and terrestrial‐breeding (viviparity) strategies. We genotyped 426 larviparous and 360 viviparous adult salamanders for 13 microsatellite loci and sequenced a mitochondrial marker for 133 larviparous and 119 viviparous individuals to compare population connectivity and landscape resistance to gene flow within a landscape genetics framework. Contrary to our predictions, viviparous populations exhibited greater differentiation and reduced genetic connectivity compared to larviparous populations. Landscape genetic analyses indicate viviparity may be partially responsible for this pattern, as water courses comprised a significant barrier only in viviparous salamanders, probably due to their fully terrestrial life cycle. Agricultural areas and, to a lesser extent, topography also decreased genetic connectivity in both larviparous and viviparous populations. This study is one of very few to explicitly demonstrate the evolution of a derived reproductive mode affects patterns of genetic connectivity. Our findings open avenues for future research to better understand the eco‐evolutionary implications underlying the emergence of terrestrial reproduction in amphibians.
Aim: Allele surfing remains poorly investigated in empirical studies due to a lack of explicit methods to detect it in natural populations. Here, we introduce a spatially explicit, sliding-window ...method to test hypotheses on how range expansions and geographic barriers impact neutral genetic structure using allele frequency data. We then use this approach to study the Ibero-Moroccan lineage of the European pond turtle, Emys orbicularis occidentalis, which recolonized the Iberian Peninsula from Africa. Location: Iberian Peninsula, Morocco. Methods: We generated a dataset of 453 genotyped individuals from 21 populations from throughout the E. o. occidentalis distribution at seven microsatellite loci. The microsatellite data were used to evaluate spatial patterns of genetic diversity and structure, as well as recent gene flow between populations. Using a spatially explicit, sliding-window approach, linear models and permutation tests, we tested for signals of allele surfing throughout the Iberian populations, including barriers to gene flow that may enhance the effect of founder events typical of range expansions. Finally, we tested for signatures of adaptation on identified surfing alleles using environmental association analysis. Results: Our study identified signatures of allele surfing throughout the range of Iberian populations. We did not find evidence that any of the loci studied are under natural selection. We therefore concluded that allele surfing has had a significant impact on genetic structure observed in E. o. occidentalis. Population isolation and fragmentation, due to habitat loss, further contribute to the present genetic differentiation between populations. Main conclusion: The sliding-window method proposed herein can help to identify alleles that underwent allele surfing at the front of range expansions. This study also highlights the role of genetic drift and geographic barriers in shaping the species' genetic structure following population range expansions. Finally, we stress the importance of evaluating the existence of allele surfing processes in biogeographic and population genetic studies, relying on allele frequency analysis, for a better interpretation of contemporary patterns of intraspecific genetic structure.
Urbanization is a severe form of habitat fragmentation that can cause many species to be locally extirpated and many others to become trapped and isolated within an urban matrix. The role of drift in ...reducing genetic diversity and increasing genetic differentiation is well recognized in urban populations. However, explicit incorporation and analysis of the demographic and temporal factors promoting drift in urban environments are poorly studied. Here, we genotyped 15 microsatellites in 320 fire salamanders from the historical city of Oviedo (Est. 8th century) to assess the effects of time since isolation, demographic history (historical effective population size; Ne) and patch size on genetic diversity, population structure and contemporary Ne. Our results indicate that urban populations of fire salamanders are highly differentiated, most likely due to the recent Ne declines, as calculated in coalescence analyses, concomitant with the urban development of Oviedo. However, urbanization only caused a small loss of genetic diversity. Regression modelling showed that patch size was positively associated with contemporary Ne, while we found only moderate support for the effects of demographic history when excluding populations with unresolved history. This highlights the interplay between different factors in determining current genetic diversity and structure. Overall, the results of our study on urban populations of fire salamanders provide some of the very first insights into the mechanisms affecting changes in genetic diversity and population differentiation via drift in urban environments, a crucial subject in a world where increasing urbanization is forecasted.
Aim
The ecological dimension of evolutionary processes has been scarcely addressed in phylogeographic studies. We reconstruct the historical biogeography of Western Mediterranean vipers to discover ...the role of climate in fostering diversification.
Location
Western Mediterranean Basin.
Taxon
Vipera aspis and Vipera latastei‐monticola complex.
Methods
We used nearly range‐wide phylogeographic analyses of three mitochondrial genes followed by geographic assignment of 4,056 records to genetic units to test phylogenetic niche conservatism, under a 3D hypervolume approach, and reconstruct paleoclimatic scenarios for the diversification of main lineages during Pleistocene.
Results
Bayesian inferences from mtDNA recovered three Miocene clades and nine Pliocene lineages that diversified during the Pleistocene. Diversification was mostly restricted to southern regions of Iberian and Italian peninsulas and to the north‐western African mountains until the late Pliocene. Some lineages expanded northwards during the Pleistocene. Accordingly, genetic diversity was higher in southern regions. Ecological niche tests mostly supported allopatric diversification with niche conservatism, although niche shifts occurred with two divergence events. Palaeoclimatic models identified particular requirements for the current distribution of main lineages and distinct responses to the cooling and warming events of the Pleistocene. Areas of climatic stability during the Pleistocene were identified for main lineages; however, climatic stability was weakly correlated with haplotype diversity.
Main conclusions
In the Western Mediterranean biodiversity hotspot, palaeo‐tectonic and palaeo‐climatic factors drove diversification since the Miocene. Comparisons among patterns of diversification, haplotype diversity, and climatic stability suggest that southern Iberian and Italian peninsulas, and north‐western African mountains acted as refugia since the Pliocene, while some northern areas favoured population persistence during the Pleistocene. Climate adaptation likely played a secondary role in the diversification of some lineages.
Ongoing global warming is disrupting several ecological and evolutionary processes, spanning different levels of biological organization. Species are expected to shift their ranges as a response to ...climate change, with relevant implications to peripheral populations at the trailing and leading edges. Several studies have analyzed the exposure of species to climate change but few have explored exposure at the intraspecific level. We introduce a framework to forecast exposure to climate change at the intraspecific level. We build on existing methods by combining correlative species distribution models, a model of species range dynamics, and a model of phylogeographic interpolation. We demonstrate the framework by applying it to 20 Iberian amphibian and reptile species. Our aims were to: (a) identify which species and intraspecific lineages will be most exposed to future climate change; (b) test if nucleotide diversity at the edges of species ranges are significantly higher or lower than on the overall range; and (c) analyze if areas of higher species gain, loss, and turnover coincide with those predicted for lineages richness and nucleotide diversity. We found that about 80% of the studied species are predicted to contract their range. Within each species, some lineages were predicted to contract their range, while others were predicted to maintain or expand it. Therefore, estimating the impacts of climate change at the species level only can underestimate losses at the intraspecific level. Some species had significant high amount of nucleotide at the trailing or leading edge, or both, but we did not find a consistent pattern across species. Spatial patterns of species richness, gain, loss, and turnover were fairly concurrent with lineages richness and nucleotide diversity. Our results support the need for increased attention to intraspecific diversity regarding monitoring and conservation strategies under climate change.
We introduce a framework to forecast exposure to climate change at the intraspecific level. We combined correlative species distribution models, a model of species range dynamics, and a model of phylogeographic interpolation. We applied the framework to 20 Iberian amphibian and reptile species. We found that about 80% of the studied species are predicted to contract their range. Within each species, some lineages were predicted to contract their range, while others were predicted to maintain or expand it. Therefore, estimating the impacts of climate change at the species level only can underestimate losses at the intraspecific level.
Aim: Investigate the role of colonization history and life history traits on contemporary patterns of genetic variation in two salamander species in a Holocene island-mainland system. Location: Rías ...Baixas, north-western Spain. Methods: We analysed mitochondrial and species-specific nuclear markers (eight microsatellite markers) in 16 populations of Salamandra salamandra and Lissotriton boscai. Contemporary gene flow patterns between mainland and island populations were evaluated by migration analyses, whereas approximate Bayesian computation (ABC) was used to assess colonization history of insular populations of both species. Results: Land bridge populations of both species exhibited reduced genetic diversity and increased genetic structure compared to mainland populations. ABC analysis showed that insular populations of both species were established by vicariance rather than by colonization via dispersal. We did not find evidence for contemporary gene flow, though the L. boscai insular population of Salvora showed genetic admixture with mainland populations. Main conclusions: This study supports the role of genetic drift in driving contemporary genetic variation of small and isolated populations. Other interplaying factors (e.g. island size, bathymetry) seemed to influence genetic variation, highlighting the importance of integrative studies to better understand the evolutionary dynamics of land bridge populations of amphibians.
Protected area systems should ideally maintain adaptive and neutral evolutionary processes. To achieve this, plans for expanding protected area systems (prioritizations) can improve coverage of ...related attributes (evolutionary attributes). However, long‐standing challenges in mapping and operationalizing evolutionary attributes have prevented their widespread usage.
We outline a novel framework for incorporating evolutionary processes into conservation planning. Using three amphibian species in the Iberian Peninsula (Hyla molleri, Pelobates cultripes and Rana iberica), we mapped a comprehensive range of adaptive and neutral evolutionary attributes to delineate places containing individuals with moderate to high heterozygosity, different neutral genetic clusters, different adaptive genetic clusters and climatic refugia. We overlaid these maps with boundaries of existing protected areas to quantify representation shortfalls and generated a prioritization to identify additional priority areas. To assess the performance of conventional approaches, we also generated a prioritization using only the species' distribution data—without the evolutionary attributes.
We found that existing protected areas within the Iberian Peninsula are failing to adequately represent evolutionary attributes for the study species. Specifically, they are not adequately representing places predicted to contain individuals with moderate to high heterozygosity for any of the studied species, and neither are they adequately representing the species' potential climatic refugia. They also have poor coverage of the distinct adaptive and neutral genetic clusters that comprise each of the species' distributions. By incorporating the evolutionary attributes into the prioritization process, we identified priority areas that would address all of the shortfalls for only a minor increase in the size of the protected area system. In comparison, the prioritization generated following conventional approaches, despite encompassing a similar extent, did not substantially improve representation of the species' evolutionary attributes.
Synthesis and applications. We introduce a framework for incorporating adaptive and neutral evolutionary processes into conservation planning. This framework can reveal weaknesses in the coverage of climatic refugia, genetic diversity and potential local adaptations by existing protected areas. Moreover, it can identify priority areas to improve conservation of evolutionary processes. Since neglecting evolutionary processes can impair conservation plans, we recommend using evolutionary data to inform decision‐making where possible.
RESUMO
As redes de áreas protegidas devem idealmente contribuir para manter os processos evolutivos adaptativos e neutros. Para isso, os planos de expansão de áreas protegidas (priorizações) podem melhorar a representação de atributos evolutivos. No entanto, o mapeamento e operacionalização desses atributos apresentam‐se como desafios de longa data que têm impedido o seu uso generalizado.
Neste trabalho propomos uma estratégia de incorporação dos processos evolutivos na identificação de áreas prioritárias para a conservação. Utilizando três espécies de anfíbios na Península Ibérica (Hyla molleri, Pelobates cultripes e Rana iberica), mapeamos um conjunto compreensivo de atributos evolutivos adaptativos e neutros, incluindo, locais contendo indivíduos com heterozigotia moderada a alta, grupos geneticamente distintos (tanto quanto a marcadores neutrais como adaptativos) e refúgios climáticos. Sobrepusemos esses mapas aos limites das áreas protegidas já existentes para quantificar o a representação actual destes locais e identificamos áreas prioritárias adicionais recorrendo a um algoritmo de optimização espacial. Para avaliar o desempenho de abordagens convencionais, identificámos áreas prioritárias para a conservação usando apenas os dados de distribuição das espécies ‐ sem os atributos evolutivos.
Constatamos que as áreas protegidas existentes na Península Ibérica não representamadequada mente os atributos evolutivos das espécies estudadas. Especificamente, estas áreas não representam adequadamente os locais previstos de conter indivíduos com heterozigotia moderada a alta para qualquer uma das espécies estudadas, nem o potencial refúgio climático das espécies. Além disso, possuem uma fraca representação dos distintos grupos genéticos, em termos adaptativos e neutros, que existem ao longo da distribuição de cada espécie. A incorporação de atributos evolutivos no processo de identificação de áreas prioritárias para a conservação permitiu identificar áreas adicionais que optimizam a sua representação. Em comparação, a priorização gerada seguindo abordagens convencionais não melhorou substancialmente a representação dos atributos evolutivos da espécie, apesar de abranger uma extensão semelhante.
Síntese e aplicações. Definimos aqui uma estratégia de inclusão dos processos evolutivos adaptativos e neutros em planos de conservação. Essa estratégia pode revelar fragilidades na cobertura de refúgios climáticos, diversidade genética e possíveis adaptações locais, pelas áreas protegidas existentes. Além disso, pode identificar áreas prioritárias para melhorar a conservação dos processos evolutivos. A não inclusão dos processos evolutivos pode comprometer a persistência das espécies, e por isso recomendamos o uso de dados evolutivos para informar tomadas de decisão sempre que possível.
We introduce a framework for incorporating adaptive and neutral evolutionary processes into conservation planning. This framework can reveal weaknesses in the coverage of climatic refugia, genetic diversity and potential local adaptations by existing protected areas. Moreover, it can identify priority areas to improve conservation of evolutionary processes. Since neglecting evolutionary processes can impair conservation plans, we recommend using evolutionary data to inform decision‐making where possible.
Explicitly accounting for phenotypic differentiation together with environmental heterogeneity is crucial to understand the evolutionary dynamics in hybrid zones. Species showing intra-specific ...variation in phenotypic traits that meet across environmentally heterogeneous regions constitute excellent natural settings to study the role of phenotypic differentiation and environmental factors in shaping the spatial extent and patterns of admixture in hybrid zones. We studied three environmentally distinct contact zones where morphologically and reproductively divergent subspecies of Salamandra salamandra co-occur: the pueriparous S. s. bernardezi that is mostly parapatric to its three larviparous subspecies neighbours. We used a landscape genetics framework to: (i) characterise the spatial location and extent of each contact zone; (ii) assess patterns of introgression and hybridization between subspecies pairs; and (iii) examine the role of environmental heterogeneity in the evolutionary dynamics of hybrid zones. We found high levels of introgression between parity modes, and between distinct phenotypes, thus demonstrating the evolution to pueriparity alone or morphological differentiation do not lead to reproductive isolation between these highly divergent S. salamandra morphotypes. However, we detected substantial variation in patterns of hybridization across contact zones, being lower in the contact zone located on a topographically complex area. We highlight the importance of accounting for spatial environmental heterogeneity when studying evolutionary dynamics of hybrid zones.
Protected‐area systems should conserve intraspecific genetic diversity. Because genetic data require resources to obtain, several approaches have been proposed for generating plans for protected‐area ...systems (prioritizations) when genetic data are not available. Yet such surrogate‐based approaches remain poorly tested. We evaluated the effectiveness of potential surrogate‐based approaches based on microsatellite genetic data collected across the Iberian Peninsula for 7 amphibian and 3 reptilian species. Long‐term environmental suitability did not effectively represent sites containing high genetic diversity (allelic richness). Prioritizations based on long‐term environmental suitability had similar performance to random prioritizations. Geographic distances and resistance distances based on contemporary environmental suitability were not always effective surrogates for identification of combinations of sites that contain individuals with different genetic compositions. Our results demonstrate that population genetic data based on commonly used neutral markers can inform prioritizations, and we could not find an adequate substitute. Conservation planners need to weigh the potential benefits of genetic data against their acquisition costs.
Evaluación de los Sustitutos de la Diversidad Genética para la Planeación de la Conservación
Resumen
Los sistemas de áreas protegidas deberían conservar la diversidad genética intraespecífica. Ya que para obtener datos genéticos se requieren recursos, se han propuesto distintas estrategias para generar los planes para los sistemas de áreas protegidas (priorizaciones) cuando los datos genéticos no están disponibles. A pesar de lo anterior, dichas estrategias basadas en sustitutos han sido poco evaluadas. Evaluamos la efectividad del potencial de las estrategias basadas en sustitutos cuya base son los datos genéticos de microsatélites obtenidos en toda la Península Ibérica y correspondientes a siete especies de anfibios y a tres de reptiles. La idoneidad ambiental a largo plazo no representó efectivamente los sitios que contienen una diversidad genética alta (riqueza de alelos). Las priorizaciones basadas en la idoneidad ambiental a largo plazo tuvieron un desempeño similar a las priorizaciones aleatorias. Las distancias geográficas y las distancias de resistencia basadas en la idoneidad ambiental contemporánea no siempre fueron sustitutos efectivos para la identificación de las combinaciones de sitios que contienen individuos con composiciones genéticas diferentes. Nuestros resultados demuestran que los datos genéticos de una población basados en marcadores neutrales de uso común pueden informar a las priorizaciones y que no pudimos encontrar un sustituto adecuado. Los planificadores de la conservación necesitan sopesar los beneficios potenciales de los datos genéticos contra sus costos de adquisición.
摘要
保护区系统应当保护物种种内的遗传多样性。然而, 由于遗传数据的获取需要较多资源, 因此, 当不能获得遗传数据时, 有几种方法可用于制定保护区系统规划 (优先排序) 。目前, 这些基于替代指标的方法尚未得到深入检测。本研究基于在伊比利亚半岛收集的7种两栖动物和3种爬行动物的微卫星遗传数据, 评估了替代方法的有效性。长期环境适宜性不能有效地代表含有高遗传多样性 (等位基因丰度) 的位点。因此, 基于长期环境适宜性进行保护优先排序的效果类似于随机排序。地理距离和基于当前环境适宜性的阻隔距离并不总能有效地作为识别含有不同遗传背景个体的位点组合的替代指标。以上研究结果表明, 基于常用中性标记的群体遗传数据可以为保护优先排序提供信息, 而我们未能找到合适的替代指标。因此, 保护规划者需要权衡基因数据的潜在效益和获取成本。【翻译: 胡怡思; 审校: 聂永刚】
Article impact statement: Conservation plans based on supposed surrogates of genetic data can perform much worse than those based directly on genetic data.
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