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Regulation of oxidative status plays a substantial role in physiological ageing. However, we know little about age-related changes of oxidative status in wild animals, and even less about the role of population history in moulding ageing rates. We addressed these questions by means of a common garden experiment, using the Tyrrhenian tree frog Hyla sarda as the study species. This species underwent a range expansion from northern Sardinia (source) up to Corsica (newly founded) during the Late Pleistocene, and then the two populations became geographically isolated. We found that, at the beginning of the experiment, Sardinian and Corsican frogs had similar concentrations of all oxidative status markers analysed. One year later, Corsican frogs had higher oxidative stress and suffered higher mortality than Sardinian frogs. Our results suggest the intriguing scenario that population differentiation in rates of physiological ageing owing to oxidative stress might be an overlooked legacy of past biogeographic processes.
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Anuros , DNA Mitocondrial , Envelhecimento , Animais , Anuros/genética , França , Itália , Estresse OxidativoRESUMO
Islands are hotspots of biodiversity, with a disproportionately high fraction of endemic lineages, often of ancient origin. Nevertheless, intra-island phylogeographies are surprisingly scarce, leading to a scanty knowledge about the microevolutionary processes induced on island populations by Plio-Pleistocene climatic oscillations, and the manner in which these processes contributed to shape their current genetic diversity. We investigated the phylogeography, historical demography and species distribution models of the Corsican endemic newt Euproctus montanus (north-western Mediterranean). As for many island endemics, the continuous distribution of E. montanus throughout its range has hitherto been considered as evidence for a single large population, a belief that also guided the species' categorization for conservation purposes. Instead, we found a geographic mosaic of ancient evolutionary lineages, with five main clades of likely Pliocene origin (2.6-5.8 My), all but one restricted to northern Corsica. Moreover, the copresence between main lineages in the same population was limited to a single case. As also suggested by growing literature on intra-island phylogeographic variation, it seems that the extensive use of simplifying assumption on the population structure and historical demography of island populations--both in theoretical and applicative studies--should be carefully reconsidered, a claim that is well exemplified by the case presented here.
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Evolução Biológica , Genética Populacional , Filogenia , Salamandridae/genética , Animais , Conservação dos Recursos Naturais , França , Geografia , Ilhas , Modelos Biológicos , Filogeografia , Dinâmica Populacional , Salamandridae/classificaçãoRESUMO
Recent empirical and theoretical studies suggest that personality and locomotory performance traits linked to dispersal abilities are crucial components of the dispersal syndromes, and that they can evolve during range expansions and colonization processes. Island colonization is one of the best characterized processes in dispersal biogeography, and its implication in the evolution of phenotypic traits has been investigated over a wide range of temporal scales. However, the effect of island colonization on personality and performance traits of natural populations, and how these traits could drive island colonization, has been little explored. Noteworthy, no studies have addressed these processes in the context of late Pleistocene range expansions. Here, we investigated the contribution of island colonization triggered by postglacial range expansions to intraspecific variation in personality and locomotory performance traits. We compared boldness, exploration, jumping performance, and stickiness abilities in populations from 3 equidistant areas of the Tyrrhenian tree frog Hyla sarda, 2 from the main island (Corsica Island), and 1 from the recently colonized island of Elba. Individuals from Elba were significantly bolder than individuals from Corsica, as they emerged sooner from a shelter (P = 0.028), while individuals from Corsica showed markedly higher jumping and stickiness performance (both P < 0.001), resulting as more performing than those of Elba. We discuss these results in the context of the major microevolutionary processes at play during range expansion, including selection, spatial sorting, founder effects, and their possible interaction with local adaptation processes.
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Dispersal is a key process in ecology and evolutionary biology, as it shapes biodiversity patterns over space and time. Attitude to disperse is unevenly distributed among individuals within populations, and that individual personality can have pivotal roles in the shaping of this attitude. Here, we assembled and annotated the first de novo transcriptome of the head tissues of Salamandra salamandra from individuals, representative of distinct behavioral profiles. We obtained 1,153,432,918 reads, which were successfully assembled and annotated. The high-quality of the assembly was confirmed by three assembly validators. The alignment of contigs against the de novo transcriptome led to a mapping percentage higher than 94%. The homology annotation with DIAMOND led to 153,048 (blastx) and 95,942 (blastp) shared contigs, annotated on NR, Swiss-Prot and TrEMBL. The domain and site protein prediction led to 9850 GO-annotated contigs. This de novo transcriptome represents reliable reference for comparative gene expression studies between alternative behavioral types, for comparative gene expression studies within Salamandra, and for whole transcriptome and proteome studies in amphibians.
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Salamandra , Transcriptoma , Animais , Perfilação da Expressão Gênica , Estudos de Associação Genética , Sequenciamento de Nucleotídeos em Larga Escala , Larva/genética , Anotação de Sequência Molecular , Salamandra/genéticaRESUMO
Understanding the genomic underpinnings of antipredatory behaviors is a hot topic in eco-evolutionary research. Yellow-bellied toad of the genus Bombina are textbook examples of the deimatic display, a time-structured behavior aimed at startling predators. Here, we generated the first de novo brain transcriptome of the Apennine yellow-bellied toad Bombina pachypus, a species showing inter-individual variation in the deimatic display. Through Rna-Seq experiments on a set of individuals showing distinct behavioral phenotypes, we generated 316,329,573 reads, which were assembled and annotated. The high-quality assembly was confirmed by assembly validators and by aligning the contigs against the de novo transcriptome with a mapping percentage higher than 91.0%. The homology annotation with DIAMOND (blastx) led to 77,391 contigs annotated on Nr, Swiss Prot and TrEMBL, whereas the domain and site protein prediction made with InterProScan led to 4747 GO-annotated and 1025 KEGG-annotated contigs. The B. pachypus transcriptome described here will be a valuable resource for further studies on the genomic underpinnings of behavioral variation in amphibians.
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Sequenciamento de Nucleotídeos em Larga Escala , Transcriptoma , Animais , Anuros , Encéfalo , Anotação de Sequência Molecular , Análise de Sequência de RNARESUMO
Assigning individuals to their source populations is crucial for conservation research, especially for endangered species threatened by illegal trade and translocations. Genetic assignment can be achieved with different types of molecular markers, but technical advantages and cost saving are recently promoting the shift from short tandem repeats (STRs) to single nucleotide polymorphisms (SNPs). Here, we designed, developed, and tested a small panel of SNPs for cost-effective geographic assignment of individuals with unknown origin of the endangered Mediterranean tortoise Testudo hermanni. We started by performing a ddRAD-seq experiment on 70 wild individuals of T. hermanni from 38 locations. Results obtained using 3182 SNPs are comparable to those previously obtained using STR markers in terms of genetic structure and power to identify the macro-area of origin. However, our SNPs revealed further insights into the substructure in Western populations, especially in Southern Italy. A small panel of highly informative SNPs was then selected and tested by genotyping 190 individuals using the KASP genotyping chemistry. All the samples from wild populations of known geographic origin were genetically re-assigned with high accuracy to the original population. This reduced SNPs panel represents an efficient molecular tool that enables individuals to be genotyped at low cost (less than 15 per sample) for geographical assignment and identification of hybrids. This information is crucial for the management in-situ of confiscated animals and their possible re-allocation in the wild. Our methodological pipeline can easily be extended to other species.
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Many temperate species experienced demographic and range contractions in response to climatic changes during Pleistocene glaciations. In this study, we investigate the evolutionary history of the Tyrrhenian tree frog Hyla sarda, a species inhabiting the Corsica-Sardinia island system (Western Mediterranean basin). We used sequence analysis of two mitochondrial (overall 1229 bp) and three nuclear (overall 1692 bp) gene fragments to assess the phylogeography and demographic history of this species, and species distribution modelling (SDM) to predict its range variation over time. Phylogeographic, historical demographic and SDM analyses consistently indicate that H. sarda does not conform to the scenario generally expected for temperate species but rather underwent demographic and range expansion mostly during the last glacial phase. Palaeogeographic data and SDM analyses suggest that such expansion was driven by the glaciation-induced increase in lowland areas during marine regression. This unusual scenario suggests that at least some temperate species may not have suffered the adverse effects of glacial climate on their population size and range extent, owing to the mitigating effects of other glaciations-induced palaeoenvironmental changes. We discuss previous clues for the occurrence of such a scenario in other species and some possible challenges with its identification. Early phylogeographic literature suggested that responses to the Pleistocene glacial-interglacial cycles were expected to vary among species and regions. Our results point out that such variation may have been greater than previously thought.
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Evolução Biológica , Ranidae/classificação , Ranidae/genética , Animais , Clima , DNA Mitocondrial/genética , Bases de Dados Genéticas , França , Variação Genética , Geografia , Haplótipos , Itália , Filogeografia , Densidade Demográfica , Análise de Sequência de DNARESUMO
The Tyrrhenian tree frog, Hyla sarda, is an amphibian endemic to the Tyrrhenian islands (Western Mediterranean). Previous investigations of its Pleistocene evolutionary history suggested that it colonised the northern portion of its current range, through a spatial diffusion process from the Sardinia island, during the last glaciation. However, southern and northern portions of the species' range experienced markedly different climatic conditions during the Late Pleistocene, suggesting the possibility of an unusual two-step process of demographic expansion. Here, we use Bayesian phylogeographic approaches to locate the ancestral area in Sardinia and to characterise better the demographic component of this expansion event. These analyses located the ancestral area for H. sarda populations along the central-eastern coast of the Sardinia island, within an area previously shown to host suitable bioclimatic conditions for H. sarda populations throughout the Late Pleistocene. Historical demographic reconstructions clearly showed that a two-step process of demographic growth fits well the data, with northern populations expanding later than Sardinia populations. The harsher climatic conditions occurred in northern islands during the glacial epoch, as compared to Sardinia, likely delayed tree frog colonisation of northern territories, and the associated demographic growth.
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Anuros/genética , Evolução Biológica , Variação Genética , Haplótipos , Filogenia , Análise de Sequência de DNA , Animais , Itália , FilogeografiaRESUMO
Genetic diversity feeds the evolutionary process and allows populations to adapt to environmental changes. However, we still lack a thorough understanding of why hotspots of genetic diversity are so 'hot'. Here, we analysed the relative contribution of bioclimatic stability and genetic admixture between divergent lineages in shaping spatial patterns of genetic diversity in the common toad Bufo bufo along the Italian peninsula. We combined population genetic, phylogeographic and species distribution modelling (SDM) approaches to map ancestral areas, glacial refugia, and secondary contact zones. We consistently identified three phylogeographic lineages, distributed in northern, central and southern Italy. These lineages expanded from their ancestral areas and established secondary contact zones, before the last interglacial. SDM identified widespread glacial refugia in peninsular Italy, sometimes located under the present-day sea-level. Generalized linear models indicated genetic admixture as the only significant predictor of the levels of population genetic diversity. Our results show that glacial refugia contributed to preserving both levels and patterns of genetic diversity across glacial-interglacial cycles, but not to their formation, and highlight a general principle emerging in Mediterranean species: higher levels of genetic diversity mark populations with substantial contributions from multiple genetic lineages, irrespective of the location of glacial refugia.
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Bufo bufo/genética , DNA Mitocondrial/genética , Variação Genética , Animais , Teorema de Bayes , Evolução Biológica , Genética Populacional , Haplótipos , Camada de Gelo , Itália , Repetições de Microssatélites/genética , Modelos Genéticos , Filogeografia , Refúgio de Vida SelvagemRESUMO
Since 2005, we have recorded annual episodes of alphaherpesvirus outbreaks in chicks of magnificent frigatebird Fregata magnificens on the Ile du Grand Connétable Nature Reserve in French Guiana. In 2009, we found sooty terns, Onychoprion fuscatus, that live sympatrically with frigatebirds, with visible clinical signs of a potential viral infection. To determine if the symptoms observed in sooty terns could be associated with an alphaherpesvirus previously identified in frigatebirds, we carried out molecular screening of samples collected from seven individuals. We identified and characterized a novel viral sequence from five birds. BLAST searches, pairwise nucleotide, and amino acid sequence comparisons, as well as phylogenetic analyses confirmed that the sequence belonged to the Herpesviridae family, of the Alphaherpesvirinae subfamily. We observed that it clustered with strains isolated from Podargidae (Caprimulgiformes), Columbiformes, and Falconiformes, but was distinct from the frigatebird herpesvirus. We have tentatively named it Onychoprion fuscatus alphaherpesvirus 1, (OfusAHV1). These two sequences, although found syntopic on the Ile du Grand Connétable, belong to two distinct alphaherpesvirus strains. Thus, the clinical symptoms showed by sooty terns do not likely result from a cross-species transmission event. Future work is needed to better characterize the virus and to investigate herpesvirus prevalence in healthy, free-ranging sooty terns, and to assess the impact of the virus on population viability.
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Discordance between mitochondrial and nuclear patterns of population genetic structure is providing key insights into the eco-evolutionary dynamics between and within species, and their assessment is highly relevant to biodiversity monitoring practices based on DNA barcoding approaches. Here, we investigate the population genetic structure of the fire salamander Salamandra salamandra in peninsular Italy. Both mitochondrial and nuclear markers clearly identified two main population groups. However, nuclear and mitochondrial zones of geographic transition between groups were located 600 km from one another. Recent population declines in central Italy partially erased the genetic imprints of past hybridization dynamics. However, the overall pattern of genetic variation, together with morphological and fossil data, suggest that a rampant mitochondrial introgression triggered the observed mitonuclear discordance, following a post-glacial secondary contact between lineages. Our results clearly show the major role played by reticulate evolution in shaping the structure of Salamandra salamandra populations and, together with similar findings in other regions of the species' range, contribute to identify the fire salamander as a particularly intriguing case to investigate the complexity of mechanisms triggering patterns of mitonuclear discordance in animals.
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Hibridização Genética , Mitocôndrias/genética , Salamandra/genética , Animais , Núcleo Celular/genética , DNA Mitocondrial/genética , Evolução Molecular , Feminino , Fluxo Gênico , Frequência do Gene , Genética Populacional , Impressão Genômica , Itália , Masculino , FilogeniaRESUMO
A correction to this article has been published and is linked from the HTML and PDF versions of this paper. The error has been fixed in the paper.
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OBJECTIVE: Species of the Baetis rhodani group are among the most widespread mayflies of the Palearctic region. However, frequent occurrence of morphologically cryptic species complicates the identification of sympatric species. Here, we proposed and tested a method for the fast, accurate, and cost-effective assignment of a large number of individuals to their putative species, based on high resolution melting profiles of a standard mitochondrial gene fragment. We tested this method using a system of three recently identified cryptic species inhabiting the Tyrrhenian Islands (western Mediterranean basin). RESULTS: Highly species-specific high resolution melting profiles were obtained, allowing the unequivocal attribution of each individual to the respective species. This assay provides a convenient and easily customizable alternative to traditional barcoding approaches, provided that the mayfly taxa occurring within the geographic area of interest have been previously identified and their high resolution melting profiles assessed.
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Ephemeroptera/classificação , Animais , Ephemeroptera/genética , Ilhas do Mediterrâneo , Reação em Cadeia da PolimeraseRESUMO
Rare hybridisations between deeply divergent animal species have been reported for decades in a wide range of taxa, but have often remained unexplained, mainly considered chance events and reported as anecdotal. Here, we combine field observations with long-term data concerning natural hybridisations, climate, land-use, and field-validated species distribution models for two deeply divergent and naturally sympatric toad species in Europe (Bufo bufo and Bufotes viridis species groups). We show that climate warming and seasonal extreme temperatures are conspiring to set the scene for these maladaptive hybridisations, by differentially affecting life-history traits of both species. Our results identify and provide evidence of an ultimate cause for such events, and reveal that the potential influence of climate change on interspecific hybridisations goes far beyond closely related species. Furthermore, climate projections suggest that the chances for these events will steadily increase in the near future.
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Mediterranean peninsulas are major biodiversity hotspots, and cold-adapted species are an important component of this biodiversity. However, cold-adapted species contributed surprisingly little to our knowledge of the intimate links between Quaternary environmental changes, species' responses to these changes, and current patterns of intraspecific biodiversity. Here, we investigated the genetic structure and evolutionary history of a cold-adapted amphibian, the Alpine newt Ichthyosaura alpestris, within the Italian peninsula. Nuclear and mitochondrial markers consistently identified three distinct genetic lineages, whose divergence dates to the Early Pleistocene (1.9 and 0.8 million years ago). Our results show that the Italian peninsula provided multiple Pleistocene refugia to this cold-adapted species, and suggest that allopatric fragmentation followed by secondary admixture have been key events in the formation of its current pattern of genetic diversity. Indeed, estimates of population genetic diversity clearly identified contact populations as those achieving the highest levels of diversity. Such concordance among cold-adapted and temperate species in terms of processes triggering the formation of regional patterns of genetic diversity provides strong support for the hypothesis that gene exchange between divergent lineages, rather than long-term stability of refugial populations, has been the main step toward the formation of hotspots of intraspecific biodiversity.
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Animal personality can be seen as behavioral polymorphism that could play a direct and active role in driving evolutionary pathways. We argue here that consistent individual differences in key personality traits affecting dispersal and other density-dependent processes have provided substantial contributions to molding biogeographic patterns. Building upon opportunities recently opened by genomics and other novel approaches, we explore the hypothesis that Pleistocene range expansions, island colonizations, and other historical biogeographic processes could have been promoted by non-random samples of behavioral types of the founder populations. We provide context and testable hypotheses, based on case studies, that could bring new implications to our understanding of the processes shaping spatial and temporal patterns of variation in animal biodiversity.
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Distribuição Animal , Comportamento Animal , Evolução Biológica , Animais , Biodiversidade , Filogenia , FilogeografiaRESUMO
How the often highly endemic biodiversity of islands originated has been debated for decades, and it remains a fervid research ground. Here, using mitochondrial and nuclear gene sequence analyses, we investigate the diversity, phylogenetic relationships, and evolutionary history of the mayfly Baetis gr. rhodani on the three largest northwestern Mediterranean islands (Sardinia, Corsica, Elba). We identify three distinct, largely co-distributed, and deeply differentiated lineages, with divergences tentatively dated back to the Eocene-Oligocene transition. Bayesian population structure analyses reveal a lack of gene exchange between them, even at sites where they are syntopic, indicating that these lineages belong to three putative species. Their phylogenetic relationships with continental relatives, together with the dating estimates, support a role for three processes contributing to this diversity: (1) vicariance, primed by microplate disjunction and oceanic transgression; (2) dispersal from the continent; and (3) speciation within the island group. Thus, our results do not point toward a prevailing role for any of the previously invoked processes. Rather, they suggest that a variety of processes equally contributed to shape the diverse and endemic biota of this group of islands.
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Spatial sorting of dispersal-enhancing traits has been implicated in substantial directional changes in the phenotypic and genotypic makeup of populations undergoing range expansion. We explore here the evolutionary consequences of such changes when two divergent lineages come into secondary contact. We combine instances from the study of contemporary range expansions and historical hybridizations, and highlight links between dispersal, sexual, and physiological traits during the non-equilibrium conditions imposed by range expansions. We argue that a stronger research focus on processes of spatial sorting of multiple traits will improve our understanding of subsequent hybridization dynamics and their evolutionary outcomes, including genomic introgression and speciation.
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Evolução Biológica , Hibridização GenéticaRESUMO
Hybridization and introgression, contrary to previous beliefs, are now considered to be widespread processes even among animal species. Nonetheless, the range of their possible outcomes and roles in moulding biodiversity patterns are still far from being fully appraised. Here we investigated the pattern of hybridization and introgression between Salamandrina perspicillata and S. terdigitata, two salamanders endemic to the Italian peninsula. Using a set of diagnostic or differentiated genetic markers (9 nuclear and 1 mitochondrial), we documented extensive unidirectional introgression of S. terdigitata alleles into the S. perspicillata gene pool in central Italy, indicating that barriers against hybridization were permeable when they came into secondary contact, and despite their ancient divergence. Nonetheless, purebred S. terdigitata, as well as F1, F2, and backcrosses were not found within the hybrid zone. Moreover, Bayesian analyses of population structure identified admixed populations belonging to a differentiated gene pool with respect to both parental populations. Overall, the observed genetic structure, together with their geographic pattern of distribution, suggests that Salamandrina populations in central Italy could have entered a distinct evolutionary pathway. How far they have gone along this pathway will deserve future investigation.