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.
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Environmental DNA (eDNA) is increasingly used for biodiversity monitoring, particularly in aquatic systems. However, each step, from sample collection to bioinformatic analysis, can introduce biases ...and influence the reliability of results. While much effort has been put into the optimization of laboratory methods, less attention has been devoted to estimate the impacts of eDNA capture methods. To address this issue, water samples were collected at nine small ponds and puddles where up to 10 amphibian species occur, using precipitation, disc filters, and capsules. We focused on targeted detection of an amphibian species, Salamandra salamandra, and on the composition of the whole amphibian community. Species detection was performed using a novel qPCR assay for S. salamandra and high‐throughput sequencing, combined with stringent versus relaxed PCR replication thresholds. Filtration techniques (disc filters and capsules) outperformed precipitation, generating a higher number of detections of S. salamandra and higher amounts of captured eDNA, while species detection was identical between disc filters and capsules. There were no significant differences between capture methods regarding amphibian community composition. The variation in detection success associated with capture methods was far higher than that associated with PCR replication, regardless of the detection method used. Our results highlight the importance of choosing a suitable capture method for eDNA studies and suggest that the choice of capture method outweighs the choice of detection method used. To the best of our knowledge, this is the first study to compare high‐capacity capsules with common eDNA methods for water samples, such as precipitation and standard disc filters.
Water samples were collected at nine small ponds using three eDNA capture methods—precipitation, disc filters, and capsules—and species detection was performed using both qPCR and high‐throughput sequencing, targeting the fire salamander Salamandra salamandra. Filtration techniques (disc filters and capsules) outperformed precipitation, generating a higher number of detections and higher amounts of captured eDNA, while species detection was identical between disc filters and capsules. The variation in detection success associated with capture methods was far higher than that associated with PCR replication, regardless of the detection method used.
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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.
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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.
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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.
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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.
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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.
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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.
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Aquatic environmental DNA is increasingly used for biodiversity monitoring, such as surveying threatened and invasive species. Mainstreaming these methods in practical applications, however, still ...requires significant standardization and optimisation, namely regarding DNA capture methods. Here we evaluated how filter type (standard disc filters vs high‐capacity capsules), number of sampling sites, volume of water filtered and environmental factors affected amphibian detection in Mediterranean temporary ponds. The study involved water filtering until clogging at one (capsules) and five (discs) sites from 16 small and shallow ponds, where three urodele and seven anuran species were recorded through sweep‐netting and adult observations. Detection probabilities were estimated from site occupancy models based on replicate sampling and from an adaptation of time‐to‐detection models relating detection probability to volume of water filtered. Discs filtered relatively small volumes (15–1250 mL), with detection probabilities of the two abundant species (Pelobates cultripes, Hyla meridionalis) increasing rapidly with sample size and water volume, reaching almost perfect detection (0.95) at four and seven discs, and 420 mL and 1860 mL, respectively. However, reaching high detection probabilities for rare species (Pelodytes atlanticus, Pleurodeles waltl, Triturus pygmaeus) would require larger sampling effort than that used in our study. Despite filtering much larger volumes (600–5300 mL), filtering with capsules at a single site per pond provided lower detection probabilities for abundant species than filtering with discs at five sites. Rarer species showed no difference between methods, which may be due to small sample sizes and reduced statistical power for species with few detections. The effect of conductivity on species detectability was largely negative, while the influence of water clarity varied across species, and pH had no effects. Overall, our results suggest that eDNA amphibian surveys in Mediterranean temporary ponds need to consider filter clogging, heterogeneous DNA distribution, and highly conductive waters.
In this study we evaluated how filter type (standard disc filters vs high‐capacity capsules), number of samples taken, volume of water filtered and environmental factors affected amphibian detection in Mediterranean temporary ponds. Discs filtered relatively small volumes, with detection probabilities of the two most abundant species increasing rapidly with sample size and water volume. Despite filtering much larger volumes, filtering with capsules at a single site per pond provided lower detection probabilities for abundant species than filtering with discs at five sites, while rarer species showed no difference between methods. Moreover, the effect of conductivity on species detectability was largely negative, while the influence of water clarity varied across species, and pH had no effects.
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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.
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