Integrating hybrid zone analyses in species delimitation: lessons from two anuran radiations of the Western Mediterranean

Dufresnes, Christophe; Pribille, Manon; Alard, Bérénice; Gonçalves, Helena; Amat, Fèlix; Crochet, Pierre‐André; Dubey, Sylvain; Perrin, Nicolas; Fumagalli, Luca; Vences, Miguel; Martínez‐Solano, Íñigo

doi:10.1038/s41437-020-0294-z

Cited by 58 publications

(51 citation statements)

References 91 publications

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“…First, the dated split (2.3-6.2 Mya) between R. t. temporaria and R. t. parvipalmata falls within the timeframe reported for other cryptic species of amphibians (3-6 My; Dufresnes, Mazepa, et al, 2019;Dufresnes et al, 2020;Dufresnes, Strachinis, et al, 2019, and references therein). Second, the hybrid zone is remarkably narrow (25 km), despite presumably weak or absent geographical barriers to dispersal in the area.…”

Section: Cryptic Speciation In a Sanctuary-type Refugiumsupporting

confidence: 61%

“…Phylogeographic surveys using high-throughput sequencing techniques can provide unprecedented insights into the history of lineages affected by Pleistocene climatic fluctuations. By clarifying the evolutionary relationships of young species complexes, and thoroughly assessing admixture between closely-related lineages, the nascent field of "genomic phylogeography" can inform on suspicions of cryptic speciation (e.g., Dufresnes et al, 2020;Dufresnes, Strachinis, et al, 2019;Hinojosa et al, 2019), and even characterize super-cryptic species, i.e., cryptic species where mtDNA barcoding is unreliable (Dufresnes, Mazepa, et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

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Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

et al. 2020

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Subdivided Pleistocene glacial refugia, best known as “refugia within refugia”, provided opportunities for diverging populations to evolve into incipient species and/or to hybridize and merge following range shifts tracking the climatic fluctuations, potentially promoting extensive cytonuclear discordances and “ghost” mtDNA lineages. Here, we tested which of these opposing evolutionary outcomes prevails in northern Iberian areas hosting multiple historical refugia of common frogs (Rana cf. temporaria), based on a genomic phylogeography approach (mtDNA barcoding and RAD‐sequencing). We found evidence for both incipient speciation events and massive cytonuclear discordances. On the one hand, populations from northwestern Spain (Galicia and Asturias, assigned to the regional endemic R. parvipalmata), are deeply‐diverged at mitochondrial and nuclear genomes (~4 My of independent evolution), and barely admix with northeastern populations (assigned to R. temporaria sensu stricto) across a narrow hybrid zone (~25 km) located in the Cantabrian Mountains, suggesting that they represent distinct species. On the other hand, the most divergent mtDNA clade, widespread in Cantabria and the Basque country, shares its nuclear genome with other R. temporaria s. s. lineages. Patterns of population expansions and isolation‐by‐distance among these populations are consistent with past mitochondrial capture and/or drift in generating and maintaining this ghost mitochondrial lineage. This remarkable case study emphasizes the complex evolutionary history that shaped the present genetic diversity of refugial populations, and stresses the need to revisit their phylogeography by genomic approaches, in order to make informed taxonomic inferences.

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Section: Cryptic Speciation In a Sanctuary-type Refugiumsupporting

confidence: 61%

Section: Introductionmentioning

confidence: 99%

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

et al. 2020

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“…Phylogeographic lineages are increasingly considered in taxonomy 8 , and when possible, their specific or subspecific rank may be decided based on whether they are (partially) reproductively isolated, following the universal biological species concept 3 . Accordingly, wide transitions are interpreted as a lack of reproductive barriers, as opposed to narrow transitions 5,71 . An ad hoc way to quantify reproductive isolation from hybrid zones is to calculate selection against hybrids from cline width w and dispersal σ, with the equations of 72 .…”

Section: Tree Frogs Admix Freely In Young Hybrid Zones But Not In Olmentioning

confidence: 99%

The effect of phylogeographic history on species boundaries: a comparative framework in Hyla tree frogs

Dufresnes

Berroneau²,

Dubey

et al. 2020

Sci Rep

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Because it is indicative of reproductive isolation, the amount of genetic introgression across secondary contact zones is increasingly considered in species delimitation. However, patterns of admixture at range margins can be skewed by the regional dynamics of hybrid zones. In this context, we posit an important role for phylogeographic history: hybrid zones located within glacial refugia (putatively formed during the Late-Pleistocene) should be better defined than those located in post-glacial or introduced ranges (putatively formed during the Holocene and the Anthropocene). We test this hypothesis in a speciation continuum of tree frogs from the Western Palearctic (Hyla), featuring ten identified contacts between species spanning Plio-Pleistocene to Miocene divergences. We review the rich phylogeographic literature of this group and examine the overlooked transition between H. arborea and H. molleri in Western France using a multilocus dataset. Our comparative analysis supports a trend that contacts zones resulting from post-glacial expansions and human translocations feature more extensive introgression than those established within refugial areas. Integrating the biogeographic history of incipient species, i.e. their age since first contact together with their genetic divergence, thus appears timely to draw sound evolutionary and taxonomic inferences from patterns of introgression across hybrid zones.

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“…Here, we adopted an integrative approach, based on the combination of CMR data and multilocus genotypes, to monitor a breeding population of the Iberian painted frog, Discoglossus galganoi Capula, Nascetti, Lanza, Bullini & Crespo, 1985(Capula et al 1985. Two major lineages occupying western and eastern Iberia have been identified in previous studies, first considered at the species level (D. galganoi and D. jeanneae) and currently as subspecies: D. g. galganoi and D. g. jeanneae (Carretero et al 2014;Dufresnes et al 2020). Populations of D. galganoi are in decline, especially in the east, where populations are highly fragmented and local extinctions have been reported in the recent past (Martínez-Solano & García-París 2002).…”

Section: Introductionmentioning

confidence: 99%

Integrative demographic study of the Iberian painted frog (Discoglossus galganoi): inter‐annual variation in the effective to census population size ratio, with insights on mating system and breeding success

2020

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In the face of worldwide amphibian declines, integrative studies combining individual-based information and genetic data represent a powerful approach to produce robust, reliable, and comparable assessments of demographic dynamics. The Iberian painted frog (Discoglossus galganoi) is endemic to Spain and Portugal and shows decreasing population trends across its range, but few studies have attempted to estimate census sizes or assess genetic diversity in wild populations, and little is known about their reproductive biology. We applied an integrative approach based on the combination of capture-mark-recapture data and multilocus genotypes to monitor a breeding population of D. galganoi in central Spain during two consecutive breeding seasons, focusing on the estimation of demographic parameters and their temporal variation. Specifically, we estimated the number of adults (N a), the effective population size (N e), and the effective number of breeders (N b), as well as survival and migration rates. We documented a >50% decrease in the estimated number of adults of both sexes between the breeding seasons of 2018 and 2019, probably associated with reduced rainfall in the latter. Estimates of N b and the N b /N a ratio were low in both seasons, with a 20-30% decrease in N b and a 47% increase in the N b /N a ratio in 2019. Based on the reconstruction of pedigrees from larval and adult genotypes, we provide the first genetic evidence of polygamy in males and females of D. galganoi and the first estimates of breeding success in the species.

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Integrating hybrid zone analyses in species delimitation: lessons from two anuran radiations of the Western Mediterranean

Cited by 58 publications

References 91 publications

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs

The effect of phylogeographic history on species boundaries: a comparative framework in Hyla tree frogs

Integrative demographic study of the Iberian painted frog (Discoglossus galganoi): inter‐annual variation in the effective to census population size ratio, with insights on mating system and breeding success

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