Historical and current patterns of gene flow in the butterfly Pararge aegeria

Abstract

Aim We have investigated the phylogeography and genetic structure of the Speckled Wood butterfly (Pararge aegeria) across its entire distribution range and studied its dispersal both on mainland and across sea straits. The apparent lack of gene flow between Sardinia and Corsica was further investigated by means of mating experiments. Location Europe and North Africa. Methods We sampled 345 individuals and sequenced one mitochondrial gene (Cytochrome c Oxidase subunit I, COI) for all samples and two nuclear genes (wingless and zerknullt) for a subset of the specimens. A total of 22 females from Corsica and Sardinia were used to establish a series of crosses to investigate reproductive compatibility and were screened for the presence of Wolbachia. Bayesian inference (BI) and haplotype networks were employed to infer phylogenetic relationships and a Principal Coordinate Analysis (PCoA) was used to represent geographical patterns of genetic diversity. Mating and courtship data were analysed using linear mixed effect models. Results We detected two main COI lineages separated by the Mediterranean Sea and maintained over relatively short sea straits. While nuclear gene variation was generally in agreement with that of COI, this was not the case in all areas (e.g. Iberian Peninsula and Corsica/Sardinia). Mating experiments revealed no evidence of reproductive isolation between the lineages, nor clear relation to Wolbachia infection status. Main conclusions We propose that following the post‐glacial recolonization of Europe, the ancestral COI lineage of P. aegeria was maintained in North Africa and Mediterranean islands, while a new lineage colonized from Eastern Europe, replacing and apparently out‐competing the ancestral variant. Several hypotheses are discussed that may explain the local discordance between the nuclear genes and COI, including sex‐specific dispersal, selection and differential rates of gene evolution.

Integrating three comprehensive data sets shows that mitochondrial DNA variation is linked to species traits and paleogeographic events in European butterflies

“…A similar regionalization was obtained by comparing butterfly communities in the same area (Dapporto, Fattorini, Vodă, Dincă, & Vila, 2014 Dapporto et al, 2017;Dincă et al, 2015;Livraghi et al, 2018). The analysis of intraspecific genetic divergence captured this main pattern, the determinants of which are still largely unexplained.…”

“…Most of the pattern obtained with intraspecific genetic variation is instead encompassed by widespread species responsible for determining similarity/dissimilarity patterns among islands and mainland. Previous studies on butterflies showed that in many cases Sardinia and Corsica differ in their populations: those populations from Corsica and Tuscan Islands mostly resemble those occurring in the Alps and the Pyrenees, whilst populations from Sardinia are often similar to those occurring in Iberia and the Balearics (e.g., Callophrys rubi , Maniola jurtina , Pararge aegeria , Coenonympha pamphilus ; Dapporto et al, ; Dincă et al, ; Livraghi et al, ). The analysis of intraspecific genetic divergence captured this main pattern, the determinants of which are still largely unexplained.…”

“…For example, a number of butterfly populations inhabiting Mediterranean islands that were connected to the mainland until the end of the last glacial period (about 15 ka) show highly diverged mtDNA compared to populations inhabiting the mainland (Dapporto et al, ). This might be due to the recent occurrence of selective sweeps or shifts of lineages along the mainland (Mallet, ; Moritz et al, ), which have not yet reached insular populations due to sea barriers (Dapporto et al, ; Livraghi et al, ). These mechanisms could maintain spatially structured populations even if their overall degree of divergence strongly changes in time.…”

Local adaptation of photoperiodic plasticity maintains life cycle variation within latitudes in a butterfly

“…It has a pan‐European distribution (Livraghi et al. ), and its life cycle varies greatly from north to south. Development may be largely aseasonal without diapause in subtropical southern populations, or seasonal and bounded by a winter spent in diapause in temperate northern populations (Nylin et al.…”

“…The speckled wood, Pararge aegeria, is a woodlandassociated satyrine butterfly with a history of use as an ecological model species (e.g., Shreeve 1986, Berwaerts et al 2002, Bergman et al 2007, Gotthard and Berger 2010, Aalberg Haugen et al 2012, Pateman et al 2016). It has a pan-European distribution (Livraghi et al 2018), and its life cycle varies greatly from north to south. Development may be largely aseasonal without diapause in subtropical southern populations, or seasonal and bounded by a winter spent in diapause in temperate northern populations (Nylin et al 1993(Nylin et al , 1995.…”