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1. Phylogeography of a cryptic speciation continuum in Eurasian spadefoot toads (Pelobates)

Author

Çetin Ilgaz, Spartak N. Litvinchuk, Dan Cogălniceanu, Nazar A. Smirnov, Galyna I. Mykytynets, Christophe Dufresnes, Paul Székely, Krzysztof Kolenda, Edvárd Mizsei, Mathieu Denoël, Jan W. Arntzen, Kamil Candan, Yusuf Kumlutaş, Petros Lymberakis, Sylvain Dubey, Márton Szabolcs, Tanja Vukov, Nicolas Perrin, Sarig Gafny, Ben Wielstra, Philippe Geniez, Nataliia Suriadna, Ilias Strachinis, Simeon Lukanov, Eli Geffen, Pierre-André Crochet, Laboratoire de Biologie de la Conservation, Département d'Ecologie et Evolution, Université de Lausanne, Natural History Museum of Crete, Department of Zoology, Tel Aviv University [Tel Aviv], Ruppin Academic Centre, Ecole pratique des hautes études, laboratoire d'Ecologie des Vertébrés, USTL Montpellier, Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry - Montpellier 3 (UM3)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut des Systèmes Intelligents et de Robotique (ISIR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Behavioural Biology Unit, Laboratory of Fish and Amphibian Ethology, Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD [France-Sud]), and Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

Subjects
Gene Flow, 0106 biological sciences, 0301 basic medicine, Sympatry, Reproductive Isolation, Genetic Speciation, Pelobates fuscus, Hybrid zones, [SDV]Life Sciences [q-bio], Speciation continuum, Allopatric speciation, [SDV.BID]Life Sciences [q-bio]/Biodiversity, Biology, Parapatric speciation, DNA, Mitochondrial, 010603 evolutionary biology, 01 natural sciences, Amphibia, Middle East, 03 medical and health sciences, Hybrid zone, Genetics, Animals, Phylogeny, ComputingMilieux_MISCELLANEOUS, Ecology, Evolution, Behavior and Systematics, Anuran, Bayes Theorem, Sequence Analysis, DNA, Reproductive isolation, biology.organism_classification, Europe, Phylogeography, Genetics, Population, 030104 developmental biology, Evolutionary biology, Hybridization, Genetic, Anura, Population genomics, Pelobates cultripes
Abstract

Cryptic phylogeographic diversifications provide unique models to examine the role of phylogenetic divergence on the evolution of reproductive isolation, without extrinsic factors such as ecological and behavioural differentiation. Yet, to date very few comparative studies have been attempted within such radiations. Here, we characterize a new speciation continuum in a group of widespread Eurasian amphibians, the Pelobates spadefoot toads, by conducting multilocus (restriction site associated DNA sequencing and mitochondrial DNA) phylogenetic, phylogeographic and hybrid zone analyses. Within the P. syriacus complex, we discovered species‐level cryptic divergences (>5 million years ago [My]) between populations distributed in the Near‐East (hereafter P. syriacus sensu stricto [s.s.]) and southeastern Europe (hereafter P. balcanicus), each featuring deep intraspecific lineages. Altogether, we could scale hybridizability to divergence time along six different stages, spanning from sympatry without gene flow (P. fuscus and P. balcanicus, >10 My), parapatry with highly restricted hybridization (P. balcanicus and P. syriacus s.s., >5 My), narrow hybrid zones (~15 km) consistent with partial reproductive isolation (P. fuscus and P. vespertinus, ~3 My), to extensive admixture between Pleistocene and refugial lineages (≤2 My). This full spectrum empirically supports a gradual build up of reproductive barriers through time, reversible up until a threshold that we estimate at ~3 My. Hence, cryptic phylogeographic lineages may fade away or become reproductively isolated species simply depending on the time they persist in allopatry, and without definite ecomorphological divergence.

Published
2019
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2. Reaching the edge of the speciation continuum: hybridization between three sympatric species of Hyla tree frogs

Author

Olivier Drillon, Pierre-André Crochet, Nicolas Perrin, Christophe Dufresnes, Guillaume Dufresnes, Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland, Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD [France-Sud]), Laboratoire de Biologie de la Conservation, Département d'Ecologie et Evolution, Université de Lausanne, Institut des Systèmes Intelligents et de Robotique (ISIR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), and Institut de Recherche pour le Développement (IRD [France-Sud])-Centre National de la Recherche Scientifique (CNRS)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université Paul-Valéry - Montpellier 3 (UM3)

Subjects
0106 biological sciences, biology, Zoology, Introgression, Hyla meridionalis, Reproductive isolation, Parapatric speciation, biology.organism_classification, Hyla, 010603 evolutionary biology, 01 natural sciences, Hybrid zone, Sympatric speciation, [SDE]Environmental Sciences, Genetic isolate, Ecology, Evolution, Behavior and Systematics, ComputingMilieux_MISCELLANEOUS
Abstract

Alloparapatric species meeting in secondary contact zones are evolutionary witnesses to how reproductive isolation progresses over time and space. Western Palearctic tree frogs (Hyla) are phenotypically similar and all the species pairs tested can hybridize and eventually admix at range margins. All except one. The early-diverged Hyla meridionalis exhibits sharp phenotypic differences: a “long” breeding call and the absence of a lateral stripe. In southwestern Europe, this species co-occurs with the “short-call” striped tree frogs H. arborea and H. molleri, two expanding lineages that admix at their parapatric margins. We estimated local gene flow between these three taxa at several syntopic breeding sites in western France. We congruently matched genotypes to phenotypes: the “short-call” striped individuals were a nuclear mixture of H. arborea and H. molleri; the “long-call” stripeless individuals all featured pure H. meridionalis nuclear ancestry and mtDNA, confirming complete genetic isolation from H. arborea/molleri. Yet, we documented an F1 hybrid between a female H. arborea/molleri and a male H. meridionalis: an incompletely-striped male with an intermediate breeding call. These findings suggest H. meridionalis is still able to reproduce with parapatric congeneric species despite 20My of divergence and strong phenotypic differentiation, but that intrinsic incompatibilities (sterility) prevent genetic introgression.

Published
2019
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3. Diversification and speciation in tree frogs from the Maghreb (Hyla meridionalis sensu lato), with description of a new African endemic

Author

Nicolas Perrin, Menad Beddek, Dmitriy V. Skorinov, Christophe Dufresnes, Luca Fumagalli, Spartak N. Litvinchuk, Pierre-André Crochet, Laboratoire de Biologie de la Conservation, Département d'Ecologie et Evolution, Université de Lausanne, Centre d’Ecologie Fonctionnelle et Evolutive (CEFE), Université Paul-Valéry - Montpellier 3 (UM3)-Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD [France-Sud])-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Politecnico di Milano [Milan] (POLIMI), Institut des Systèmes Intelligents et de Robotique (ISIR), Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Université Paul-Valéry - Montpellier 3 (UPVM)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut de Recherche pour le Développement (IRD [France-Sud]), and Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland

Subjects
0106 biological sciences, 0301 basic medicine, Genetic Speciation, [SDV]Life Sciences [q-bio], Fauna, Lineage (evolution), Zoology, Tree frog, [SDV.BID]Life Sciences [q-bio]/Biodiversity, [SDV.BID.SPT]Life Sciences [q-bio]/Biodiversity/Systematics, Phylogenetics and taxonomy, 010603 evolutionary biology, 01 natural sciences, DNA, Mitochondrial, 03 medical and health sciences, Sensu, Africa, Northern, Genetics, Animals, Molecular Biology, ComputingMilieux_MISCELLANEOUS, Ecology, Evolution, Behavior and Systematics, Phylogeny, Cell Nucleus, Principal Component Analysis, biology, Genetic Variation, Hyla meridionalis, Reproductive isolation, biology.organism_classification, Mitochondria, Phylogeography, 030104 developmental biology, Genetics, Population, Anura
Abstract

Comparative molecular studies emphasized a new biogeographic paradigm for the terrestrial fauna of North Africa, one of the last uncharted ecoregions of the Western Palearctic: two independent east-west divisions across the Maghreb. Through a comprehensive phylogeography, we assessed how this model suits the genetic diversification documented for the tree frog Hyla meridionalis sensu lato. Analyses of mtDNA variation and thousands of nuclear loci confirmed the old split (low-Pliocene) between Tunisian and Algerian populations. These lineages meet but barely admix in the eastern Maghreb (Algerian-Tunisian border), a sign of putatively advanced reproductive isolation. In the western Maghreb, we report a Pleistocene divergence between Moroccan and Algerian populations. Tree frogs thus follow both predictions: a double east-west break that gave rise to two suture zones characteristic of North-African phylogeography. Moreover, some intraspecific mtDNA variation is not mirrored by the nuclear data, emphasizing that evolutionary units should always be designated by multilocus approaches. Last but not least, we describe the Tunisian lineage as a new species endemic to Africa.

Published
2018
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4. Stocking activities for the arctic charr in lake geneva: genetic effects in space and time

Author

Nicolas Perrin, Arnaud Caudron, Romain Savary, Luca Fumagalli, Alexis Champigneulle, Sylvain Dubey, Christophe Dufresnes, Laboratoire de Biologie de la Conservation, Département d'Ecologie et Evolution, Université de Lausanne, Centre Alpin de Recherche sur les Réseaux Trophiques et Ecosystèmes Limniques (CARRTEL), Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])-Institut National de la Recherche Agronomique (INRA), Science-Management Interface for Biodiversity Conservation (SCIMABIO Interface), Hintermann and Weber, Federal Office for the Environment (FOEN), Switzerland, Inspection de la peche du Canton de Vaud, Switzerland, Ministere de l'Ecologie, de l'Energie, du Developpement Durable et de la Mer, France, Haute-Savoie Departmental Federation of Fisheries, France, La Maison de la Riviere, Tolochenaz, Switzerland, and Institut National de la Recherche Agronomique (INRA)-Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])

Subjects
0106 biological sciences, microsatellite, Biodiversité et Ecologie, Population, Salmonids, Salvelinus, conservation‐based stocking programs, fisheries management, genetic bottleneck, genetic integrity, historical DNA, microsatellites, stockage, Context (language use), 010603 evolutionary biology, 01 natural sciences, Biodiversity and Ecology, storage, Stocking, Genetic variation, Lac Léman, salmonides, conservation-based stocking programs, 14. Life underwater, education, Salmonid, Ecology, Evolution, Behavior and Systematics, genêtic effects, Nature and Landscape Conservation, Original Research, education.field_of_study, Genetic diversity, Ecology, biology, 010604 marine biology & hydrobiology, fisherie management, biology.organism_classification, arctique, Population bottleneck, effet génétique, Genetic structure, [SDE.BE]Environmental Sciences/Biodiversity and Ecology
Abstract

Artificial stocking practices are widely used by resource managers worldwide, in order\ud to sustain fish populations exploited by both recreational and commercial activities,\ud but their benefits are controversial. Former practices involved exotic strains, although\ud current programs rather consider artificial breeding of local fishes (supportive breeding).\ud Understanding the complex genetic effects of these management strategies is an\ud importan t challenge with economic and conservation implications, especially in the\ud context of population declines. In this study, we focus on the declining Arctic charr\ud (Salvelinus alpinus) population from Lake Geneva (Switzerland and France), which has\ud initially been restocked with allochtonous fishes in the early eighties, followed by supportive\ud breeding. In this context, we conducted a genetic survey to document the\ud evolution of the genetic diversity and structure throughout the last 50 years, before\ud and after the initiation of hatchery supplementation, using contemporary and historical\ud samples. We show that the introduction of exotic fishes was associated with a genetic\ud bottleneck in the 1980–1990s, a break of Hardy–Weinberg Equilibrium (HWE),\ud a reduction in genetic diversity, an increase in genetic structure among spawning sites,\ud and a change in their genetic composition. Together with better environmental conditions,\ud three decades of subsequent supportive breeding using local fishes allowed to\ud re-establish HWE and the initial levels of genetic variation. However, current spawning\ud sites have not fully recovered their original genetic composition and were extensively\ud h omogenized across the lake. Our study demonstrates the drastic genetic\ud consequ e nces of different restocking tactics in a comprehensive spatiotemporal\ud framewo rk and suggests that genetic alteration by nonlocal stocking may be partly\ud reversible through supportive breeding. We recommend that conservation-based programs\ud consider local diversity and implement adequate protocols to limit the genetic\ud homogenization of this Arctic charr population.

Published
2017
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5. Evidence for morphological and adaptive genetic divergence between lake and stream habitats in European minnows (Phoxinus phoxinus, Cyprinidae).

Author

Collin H and Fumagalli L

Subjects
Adaptation, Physiological genetics, Adaptation, Physiological physiology, Amplified Fragment Length Polymorphism Analysis, Animals, Genetic Drift, Genotype, Selection, Genetic genetics, Selection, Genetic physiology, Cyprinidae genetics, Cyprinidae physiology, Ecosystem, Lakes, Rivers
Abstract

Natural selection drives local adaptation, potentially even at small temporal and spatial scales. As a result, adaptive genetic and phenotypic divergence can occur among populations living in different habitats. We investigated patterns of differentiation between contrasting lake and stream habitats in the cyprinid fish European minnow (Phoxinus phoxinus) at both the morphological and genomic levels using geometric morphometrics and AFLP markers, respectively. We also used a spatial correlative approach to identify AFLP loci associated with environmental variables representing potential selective forces responsible for adaptation to divergent habitats. Our results identified different morphologies between lakes and streams, with lake fish presenting a deeper body and caudal peduncle compared to stream fish. Body shape variation conformed to a priori predictions concerning biomechanics and swimming performance in lakes vs. streams. Moreover, morphological differentiation was found to be associated with several environmental variables, which could impose selection on body and caudal peduncle shape. We found adaptive genetic divergence between these contrasting habitats in the form of 'outlier' loci (2.9%) whose genetic divergence exceeded neutral expectations. We also detected additional loci (6.6%) not associated with habitat type (lake vs. stream), but contributing to genetic divergence between populations. Specific environmental variables related to trophic dynamics, landscape topography and geography were associated with several neutral and outlier loci. These results provide new insights into the morphological divergence and genetic basis of adaptation to differentiated habitats., (© 2011 Blackwell Publishing Ltd.)

Published
2011
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6. Molecular phylogeography of the nose-horned viper (Vipera ammodytes, Linnaeus (1758)): evidence for high genetic diversity and multiple refugia in the Balkan peninsula.

Author

Ursenbacher S, Schweiger S, Tomović L, Crnobrnja-Isailović J, Fumagalli L, and Mayer W

Subjects
Animals, Bulgaria, Croatia, Cytochromes b genetics, DNA, Mitochondrial chemistry, DNA, Mitochondrial genetics, Genetic Variation, Geography, Greece, Italy, Molecular Sequence Data, RNA, Ribosomal, 16S genetics, Sequence Analysis, DNA, Slovenia, Turkey, Viperidae classification, Yugoslavia, Phylogeny, Viperidae genetics
Abstract

The nose-horned viper (Vipera ammodytes) occurs in a large part of the south-eastern Europe and Asia Minor. Phylogenetic relationships were reconstructed for a total of 59 specimens using sequences from three mitochondrial regions (16S and cytochrome b genes, and control region, totalling 2308 bp). A considerable number of clades were observed within this species, showing a large genetic diversity within the Balkan peninsula. Splitting of the basal clades was evaluated to about 4 million years ago. Genetic results are in contradiction with presently accepted taxonomy based on morphological characters: V. a. gregorwallneri and V. a. ruffoi do not display any genetic difference compared with the nominotypic subspecies (V. a. ammodytes), involving that these subspecies can be regarded as synonyms. High genetic divergence in the central part of the Balkan peninsula is not concordant with low morphological differentiation. Finally, the extensive genetic diversity within the Balkan peninsula and the colonisation routes are discussed.

Published
2008
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7. Phylogeography and Pleistocene refugia of the adder (Vipera berus) as inferred from mitochondrial DNA sequence data.

Author

Ursenbacher S, Carlsson M, Helfer V, Tegelström H, and Fumagalli L

Subjects
Animals, Asia, Base Sequence, Cluster Analysis, Cytochromes b chemistry, Cytochromes b genetics, DNA, Mitochondrial chemistry, Europe, Genetic Variation, Locus Control Region genetics, Molecular Sequence Data, Phylogeny, Sequence Alignment, Sequence Analysis, DNA, DNA, Mitochondrial genetics, Ecosystem, Viperidae genetics
Abstract

In order to contribute to the debate about southern glacial refugia used by temperate species and more northern refugia used by boreal or cold-temperate species, we examined the phylogeography of a widespread snake species (Vipera berus) inhabiting Europe up to the Arctic Circle. The analysis of the mitochondrial DNA (mtDNA) sequence variation in 1043 bp of the cytochrome b gene and in 918 bp of the noncoding control region was performed with phylogenetic approaches. Our results suggest that both the duplicated control region and cytochrome b evolve at a similar rate in this species. Phylogenetic analysis showed that V. berus is divided into three major mitochondrial lineages, probably resulting from an Italian, a Balkan and a Northern (from France to Russia) refugial area in Eastern Europe, near the Carpathian Mountains. In addition, the Northern clade presents an important substructure, suggesting two sequential colonization events in Europe. First, the continent was colonized from the three main refugial areas mentioned above during the Lower-Mid Pleistocene. Second, recolonization of most of Europe most likely originated from several refugia located outside of the Mediterranean peninsulas (Carpathian region, east of the Carpathians, France and possibly Hungary) during the Mid-Late Pleistocene, while populations within the Italian and Balkan Peninsulas fluctuated only slightly in distribution range, with larger lowland populations during glacial times and with refugial mountain populations during interglacials, as in the present time. The phylogeographical structure revealed in our study suggests complex recolonization dynamics of the European continent by V. berus, characterized by latitudinal as well as altitudinal range shifts, driven by both climatic changes and competition with related species.

Published
2006
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