Secondary contact zones of closely‐related Erebia butterflies overlap with narrow phenotypic and parasitic clines

Abstract

Zones of secondary contact between closely related taxa are a common legacy of the Quaternary ice ages. Despite their abundance, the factors that keep species apart and prevent hybridization are often unknown. Here, we study a very narrow contact zone between three closely related butterfly species of the Erebia tyndarus species complex. Using genomic data, we first determined whether gene flow occurs and then assessed whether it might be hampered by differences in chromosome number between some species. We found interspecific gene flow between sibling species that differ in karyotype by one chromosome. Conversely, only F1 hybrids occurred between two species that have the same karyotype, forming a steep genomic cline. In a second step, we fitted clines to phenotypic, ecological and parasitic data to identify the factors associated with the genetic cline. We found clines for phenotypic data and the prevalence of the endosymbiont parasite Wolbachia to overlap with the genetic cline, suggesting that they might be drivers for separating the two species. Overall, our results highlight that some gene flow is possible between closely related species despite different chromosome numbers, but that other barriers restrict such gene flow.

Prevalence and relationship of endosymbiotic Wolbachia in the butterfly genus Erebia

“…The prevalence was particularly low in the subspecies isarica of E. euryale (14%, Fig. 2 ) as well as in E. tyndarus , confirming earlier observations [ 18 ]. For E. cassioides —the host species of our sequenced Wolbachia genome—the Wolbachia prevalence was high for specimens from the Alps (87.9%).…”

“…Exceptions were E. vogesiaca that were sampled in the Vosges (France) and few E. cassioides that were collected in the Apennines (Italy) or Pyrenees (France, Spain) [ 28 ]. Because former studies suggested that populations of E. cassioides from geographically distinct mountain ridges likely originate from different glacial refugia [ 18 , 23 , 28 ], we treated them as separate lineages in the subsequent analyses.

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“…However, to which degree Wolbachia may have contributed to the spectacular diversification of Lepidoptera remains elusive. Divergent Wolbachia infections may for example act as a barrier to gene flow upon secondary contact between closely related host lineages or species [ 16 ], as has been suggested in some cases [ 17 , 18 ]. A first step to assess the potential evolutionary implications of Wolbachia is the quantification of its prevalence and differentiation among closely related host species.…”

“…The diversification of Erebia has been associated with differentiation in distinct glacial refugia as a consequence of the Quaternary glacial cycles [ 21 – 23 ]. While distantly related species often coexist and exploit different microhabitats following their postglacial range expansions [ 19 , 24 ], in several cases closely related species or lineages exclude each other by forming very narrow secondary contact zones [ 18 , 19 ]. Despite their broad Palearctic distribution, relatively little is known about the diversity and actual impact of Wolbachia in this host genus.…”

“…Despite their broad Palearctic distribution, relatively little is known about the diversity and actual impact of Wolbachia in this host genus. In the case of E. tyndarus and E. cassioides , the secondary contact zone manifests as a very narrow genomic cline in the central Alps with only few F1 hybrid individuals, suggesting selection against interspecific gene flow in this system [ 18 ]. Wolbachia might represent an important barrier separating the two species, given that the genomic cline overlaps with changes in Wolbachia prevalence: While more than 90% of E. cassioides , including the putative F1 hybrids, were infected , none of the studied E. tyndarus specimens carried Wolbachia in the contact zone [ 18 ].…”