Prevalence and relationship of endosymbiotic Wolbachia in the butterfly genus Erebia

Abstract

Background Wolbachia is an endosymbiont common to most invertebrates, which can have significant evolutionary implications for its host species by acting as a barrier to gene flow. Despite the importance of Wolbachia, still little is known about its prevalence and diversification pattern among closely related host species. Wolbachia strains may phylogenetically coevolve with their hosts, unless horizontal host-switches are particularly common. We address these issues in the genus Erebia, one of the most diverse Palearctic butterfly genera. Results We sequenced the Wolbachia genome from a strain infecting Erebia cassioides and showed that it belongs to the Wolbachia supergroup B, capable of infecting arthropods from different taxonomic orders. The prevalence of Wolbachia across 13 closely related Erebia host species based on extensive population-level genetic data revealed that multiple Wolbachia strains jointly infect all investigated taxa, but with varying prevalence. Finally, the phylogenetic relationships of Wolbachia strains are in some cases significantly associated to that of their hosts, especially among the most closely related Erebia species, demonstrating mixed evidence for phylogenetic coevolution. Conclusions Closely related host species can be infected by closely related Wolbachia strains, evidencing some phylogenetic coevolution, but the actual pattern of infection more often reflects historical or contemporary geographic proximity among host species. Multiple processes, including survival in distinct glacial refugia, recent host shifts in sympatry, and a loss of Wolbachia during postglacial range expansion seem to have jointly shaped the complex interactions between Wolbachia evolution and the diversification of its host among our studied Erebia species.

Secondary contact rather than coexistence— Erebia butterflies in the Alps

“…Although the potential role of Wolbachia in Erebia is still unknown (Lucek et al 2021), it may act as an intrinsic postzygotic barrier to gene flow, potentially causing sterility of hybrids as in other butterflies (Nice et al 2009). Indeed, E. tyndarus can be crossed with moderate success with E. cassioides when for the latter a distinct lineage from the Eastern Alps is used (Lorkovic 1958) that shares a Wolbachia strain with nearby E. tyndarus populations (Lucek et al 2021). The genomic cline also overlapped with a phenotypic cline on wing patterns (Lucek et al 2020).…”

Mitochondrial DNA-based phylogeography of the large ringlet Erebia euryale (Esper, 1805) suggests recurrent Alpine-Carpathian disjunctions during Pleistocene (Nymphalidae, Satyrinae)

“…There is, however, no doubt that additional genomic data in future work will enhance the resolution of the relationships and of the timing of splitting events. The use of nuclear genomic data would also address the possibility that the divergences we detected in COI have been influenced by Wolbachia infections, which have been detected in E. Euryale too (Ritter et al 2013;Lucek et al 2021).…”

Climatic niche conservatism and ecological diversification in the Holarctic cold-dwelling butterfly genusErebia

“…The origin of alpine endemic insects has complex drivers (Queiroz et al 2022), including allopatric speciation (Schoville and Roderick, 2010, Schat et al 2022, Todisco et al 2010), diversity dependent radiation (Condamine 2018), or interactions with endosymbionts (Lucek et al 2021, Weng et al 2021). We fill in new information into the mosaic describing diversification drivers of alpine insects in relation to the role of the evolution of their climatic niches.…”

“…The adaptive scenario is supported by climatic niche differentiation and contrasting microhabitat use observed in sympatric butterflies (Kleckova et al 2014). In contrast, the studies of Erebia secondary zones suggest preceding allopatric differentiation connected with coevolution with endosymbionts (Lucek et al 2021). To shed more light on processes driving the diversification of Erebia , we ask three sets of questions in this study:…”

“…Here, we ask whether the evolutionary history of a species-rich group of temperate cold-dwelling butterflies is determined by niche conservatisms or rather by adaption to distinct climatic niches among lineages. Studies of Erebia secondary contact zones suggest preceding allopatric differentiation connected with coevolution with endosymbionts (Lucek et al 2021). To shed more light on processes driving the diversification of Erebia at the macroevolutionary and macroecological scales, we ask three sets of questions in this study: Did species’ climatic niches evolve gradually following the niche conservatism hypothesis or rapidly during the early evolution of the genus in congruence with the adaptive radiation scenario?…”