Two consecutive Wolbachia‐mediated mitochondrial introgressions obscure taxonomy in Palearctic swallowtail butterflies (Lepidoptera, Papilionidae)

Abstract

Swallowtail butterflies (Papilionidae) are among the most spectacular and well‐known Lepidoptera in the European fauna, but their systematics is not fully elucidated. A notable case is that of Iphiclides feisthamelii which, after more than 180 years since description, still has a debated status, being often considered as a subspecies of Iphiclides podalirius. To elucidate the relationship between the two taxa and the evolutionary processes that led to their separation, we combine mitochondrial and nuclear DNA (mtDNA and nDNA) data, Wolbachia screening, genitalia morphology and wing UV reflectance. Our results show that the two taxa clearly differ in male and female genital morphology, male wing UV reflectance and nDNA. Two Wolbachia strains were found to widely infect the studied samples, apparently explaining the phylogeographic pattern displayed by mtDNA. The available data point towards a historical Wolbachia infection that spread from I. podalirius to I. feisthamelii and produced a mitochondrial introgression. Currently, a new Wolbachia strain is spreading across mainland populations of I. podalirius, mediating once more a mitochondrial genetic sweep, which has already infected and introgressed I. feisthamelii populations in south‐eastern France. We conclude that, given the marked differences in morphology and nDNA between the two taxa, and the apparent restriction of hybridization to a narrow contact area where non‐hybrid specimens are common, the taxon feisthamelii should be considered as a separate species. Within this species, two well‐differentiated nDNA lineages that represent European and Maghrebian populations are documented, here proposed as subspecies. The case of, presumably, two consecutive Wolbachia‐mediated mitochondrial introgression events, further supports the view that infection by this endosymbiont may be frequently related to mito‐nuclear discordance in insects.

The Pleistocene species pump past its prime: evidence from European butterfly sister species

“…Such sweeps may be acting on mt variation directly or, indirectly, through maternally inherited genomes or chromosomes (e.g. Wolbachia (Jiggins, 2003) and the W chromosome) and have been documented in a number of Lepidopteran systems (Gaunet et al, 2019a, Graham & Wilson, 2012, Kodandaramaiah et al, 2013, Martin et al, 2020, Ritter et al, 2013.…”

The conundrum of species delimitation: a genomic perspective on a mitogenetically super-variable butterfly

“…As a matter of fact, M. didyma is one of the few documented cases among European butterflies (e.g. genus Lysandra [54], Iphiclides podalirius and I. feisthamelii [55], Melitaea phoebe and M. ornata [56], genus Brenthis [57], Thymelicus sylvestris [14]) where mito-nuclear discordance is caused by biological processes, and not by operational factors (e.g. misidentifications, deficient taxonomy), although the latter have been shown to represent an important bias in European Lepidoptera [58].…”

Assigning occurrence data to cryptic taxa improves climatic niche assessments: Biodecrypt, a new tool tested on European butterflies

“…Of these, we compiled sufficient identified records for 16 cases amalgamated in the above‐mentioned atlas, which represent 33 cryptic species. These species were used in this study: (a) Carcharodus alceae and Carcharodus tripolinus , which co‐exist in southern Iberia (Dincă et al., 2015); (b) Spialia sertorius and Spialia rosae , largely sympatric in Iberia (Hernández‐Roldán et al, 2016); (c) Pyrgus malvae and Pyrgus malvoides , parapatric with a contact zone along central France and the Alps (Koren, Beretta, Črne, & Verovnik, 2013; Litman et al., 2018); (d) Iphiclides podalirius and Iphiclides feisthamelii , parapatric with a contact zone in the Pyrenees and southern France (Gaunet et al., 2019; Wiemers & Gottsberger, 2010); (e) Zerynthia polyxena and Zerynthia cassandra , parapatric with a contact zone in northern Italy (Zinetti et al., 2013); (f) Pontia daplidice and Pontia edusa , parapatric with a contact zone in north‐western Italy (Porter, Wenger, Geiger, Scholl, & Shapiro, 1997); (g) Leptidea sinapis/reali/juvernica , with L. reali and L. juvernica being allopatric, but each sympatric with respect to L. sinapis (Dincă, Lukhtanov, et al., 2011, Dinca et al, 2013); (h) Lycaena tityrus and Lycaena bleusei , parapatric in Iberia (Dincă et al., 2015); (i) Polyommatus icarus and Polyommatus celina , parapatric with contact in southern Iberia (Dincă, Dapporto, & Vila, 2011); (j) Lysandra coridon and Lysandra caelestissima , parapatric in central Iberia (Talavera, Lukhtanov, Rieppel, Pierce, & Vila, 2013); (k) Melitaea athalia and Melitaea celadussa , parapatric with a contact zone from southern France through the Alps. We also applied the assignment procedure to a series of species showing almost complete allopatric distribution that were split in Wiemers et al.…”