Roberta Bisconti

Multiple lines of evidence for demographic and range expansion of a temperate species (Hyla sarda) during the last glaciation

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.

Bolder Takes All? The Behavioral Dimension of Biogeography

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.

The Tangled Evolutionary Legacies of Range Expansion and Hybridization

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.

Has Living on Islands Been So Simple? Insights from the Insular Endemic Frog Discoglossus montalentii

Island populations have been extensively used as model systems in ecology, biogeography, conservation and evolutionary biology, owing to the several simplifying assumptions that they allow. Nevertheless, recent findings from intra-island phylogeographic studies are casting doubts on the generality of some of these underlying assumptions. We investigated the phylogeography, historical demography, and population genetic structure of the Corsican endemic frog, Discoglossus montalentii. In contrast with expectations based on its insular, restricted and continuous distribution, we found evidence of 3 phylogroups, whose rather ancient divergence (Early-Middle Pleistocene) was likely primed by climatic changes that occurred during the ‘middle Pleistocene revolution’. Furthermore, their differentiation explained most (68%) of the overall genetic diversity that was observed. These results and the growing evidence from intra-island phylogeographies, suggest that island populations frequently may not conform to some long-standing assumptions, including long-term stability, range-wide panmixia and the correlation of effective population size to the island size. As a consequence, both for theoretical and for applied purposes, the extensive use of these assumptions in the study of island populations warrants a careful re-examination.

Extensive unidirectional introgression between two salamander lineages of ancient divergence and its evolutionary implications

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.

Cryptic diversity and multiple origins of the widespread mayfly species group Baetis rhodani (Ephemeroptera: Baetidae) on northwestern Mediterranean islands

Abstract 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.

Quaternary history, population genetic structure and diversity of the cold-adapted Alpine newt Ichthyosaura alpestris in peninsular Italy

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.

Historical Biogeography and the (Epi)Genetic Architecture of Animal Personality: A Comment on Cobben and van Oers

In their comment on our recent TREE article on the implications of animal personality for biogeographical patterns [1], Cobben and van Oers [2] emphasise the contribution of heritable epigenetic variation to personality phenotypes. They highlight challenges in investigating such contribution in a historical perspective, delineate consequential research questions, and propose intriguing avenues to circumvent these challenges. We wholeheartedly welcome Cobben and van Oerss contribution [2] to the discussion we sought to stimulate.

Drilling down hotspots of intraspecific diversity to bring them into on-ground conservation of threatened species

Unprecedented rates of biodiversity loss rise the urgency for preserving species ability to cope with ongoing global changes. An approach in this direction is to target intra-specific hotspots of genetic diversity as conservation priorities. However, these hotspots are often identified by sampling at a spatial resolution too coarse to be useful in practical management of threatened species, hindering the long-appealed dialog between conservation stakeholders and conservation genetic researchers. Here, we investigated the spatial and temporal variation in species presence, genetic diversity, as well as potential risk factors, within a previously identified hotspot of genetic diversity for the endangered Apennine yellow bellied toad Bombina pachypus. Our results show that this hotspot is neither a geographically homogeneous nor a temporally stable unit. Over a time-window spanning 10-40 years since previous assessments, B. pachypus populations declined in large portions of its hotspot, and their genetic diversity levels decreased. Considering the demographic trend, genetic and epidemiological data, and models of current and future climatic suitability, populations at the extreme south of the hotspot area still qualify for urgent in-situ conservation actions, whereas northern populations would be better managed through a mix of in-situ and ex-situ actions. Our results emphasize that identifying hotspot of genetic diversity, albeit essential step, does not suffice to warrant on-ground conservation of threatened species. Hotspots should be analysed at finer geographic and temporal scales, to provide conservation stakeholders with key knowledge to best define conservation priorities, and to optimize resource allocation to alternative management practices.

Hybridization and extensive mitochondrial introgression among fire salamanders in peninsular Italy

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.