Hybrid zone formation and contrasting outcomes of secondary contact over transects in common toads

Abstract

Much progress in speciation research stems from documenting patterns of morphological and genetic variation in hybrid zones. Contrasting patterns of marker introgression in different sections of the contact can provide valuable insights on the relative importance of various evolutionary mechanisms maintaining species differences in the face of hybridization and gene flow and on hybrid zone temporal and spatial dynamics. We studied species interactions in the common toads Bufo bufo and B. spinosus in France and northwestern Italy using morphological and molecular data from the mitochondrial and nuclear genomes in an extensive survey, including two independent transects west and east of the Alps. At both, we found sharp, coincident and concordant nuclear genetic transitions. However, morphological clines were wider or absent and mtDNA introgression was asymmetric. We discuss alternative, nonexclusive hypotheses about evolutionary processes generating these patterns, including drift, selection, long-distance dispersal and spatial shifts in hybrid zone location and structure. The distribution of intraspecific mtDNA lineages supports a scenario in which B. bufo held a local refugium during the last glacial maximum. Present-day genetic profiles are best explained by an advance of B. spinosus from a nearby Iberian refugium, largely superseding the local B. bufo population, followed by an advance of B. bufo from the Balkans, with prongs north and south of the Alps, driving B. spinosus southwards. A pendulum moving hybrid zone, first northwards and then southwards, explains the wide areas of introgression at either side of the current position of the contact zones.

Testing an hypothesis of hybrid zone movement for toads in France

“…We examined patterns of gene flow and admixture linkage disequilibrium to test the hypothesis of movement of the hybrid zone in two common toad species ( B. bufo and B. spinosus ) in northwest France. Introgression from B. spinosus into B. bufo was more frequent than introgression the other way around, a result that was found before with four nuclear markers (Arntzen et al, ). Disregarding whether cline model fits are significant, eleven markers show introgression from B. spinosus into B. bufo and two show introgression the other way around, a significant difference (Chi‐square test for equal probabilities, χ 2 = 6.23, p = 0.013).…”

“…In conclusion, we cannot reject the null hypothesis of a stable Bufo hybrid zone in northwest France, and low levels of dispersal and random genetic drift due to small population sizes are important in shaping the patterns of introgression. Based on earlier studies, this hybrid zone was predicted to move southwards (Arntzen et al, ). Our data set shows similar characteristics to those of previous studies (e.g., northward introgression), but with additional analyses we showed asymmetric reproductive isolation may provide a more important driver of asymmetric introgression than hybrid zone movement.…”

“…Displaced and discordant clines exist in many species, both for nuclear and mitochondrial markers, and may be caused by sex‐biased gene flow or by adaptive introgression (Bonnet, Leblois, Rousset, & Crochet, ; Excoffier, Foll, & Petit, ; Mallet, ; Sloan, Havird, & Sharbrough, ; Toews & Brelsford, ; While et al, ). However, displaced and discordant clines may also be caused by hybrid zone movement, when a trail of genetic material from the overtaken species remains present in the overtaking species (Arntzen, de Vries, Canestrelli, & Martínez‐Solano, ; Excoffier et al, ; Gay, Crochet, Bell, & Lenormand, ; Rohwer, Bermingham, & Wood, ; Wielstra, Burke, Butlin, Avcı et al, ).…”

“…Based on four nuclear gene coding markers, twelve microsatellites, and two mitochondrial SNP markers, the width of the hybrid zone (30 km) compared to the dispersal distance (1.3 km/generation) suggested that selection against hybrids restricts gene flow through the hybrid zone (Arntzen et al, ). In the southeast of France, the Bufo hybrid zone was hypothesised to move southwards based on traces of introgression of one nuclear gene coding marker (of four tested), and discordance between nuclear, mtDNA, and morphological clines (Arntzen et al, ). In the northwest of France, a similar data set including microsatellite data, showed introgression towards the north in two nuclear markers out of four, but was not analysed from the perspective of hybrid zone movement at the time (Arntzen et al, ).…”

Transgressive niche across a salamander hybrid zone revealed by microhabitat analyses

“…Nevertheless, hybrid zones often occur along ecological gradients, where transitional environments may allow the contact between species with different niches (Culumber, Shepard, Coleman, Rosenthal, & Tobler, ). Under these circumstances, the hybrid zone can be maintained if hybrids exploit intermediate niches along environmental gradients (Arntzen et al, ; Johannesson et al, ). However, the situation is completely different when hybrids occupy transgressive niches and are able to exploit habitat that are unsuitable for either parental species.…”