Genomics Reveal Admixture and Unexpected Patterns of Diversity in a Parapatric Pair of Butterflies.

Mohadeseh Sadat Tahami,Leonardo Dapporto,Peter Huemer,Vlad Dincă,Kyung Min Lee,Roger Vila,Maria Heikkilä,Mukta Joshi,Sarah Schmid,Marko Mutanen

doi:10.3390/genes12122009

Abstract

We studied the evolutionary relationship of two widely distributed parapatric butterfly species, Melitaea athalia and Melitaea celadussa, using the ddRAD sequencing approach, as well as genital morphology and mtDNA data. M. athalia was retrieved as paraphyletic with respect to M. celadussa. Several cases of mito-nuclear discordance and morpho-genetic mismatch were found in the contact zone. A strongly diverged and marginally sympatric clade of M. athalia from the Balkans was revealed. An in-depth analysis of genomic structure detected high levels of admixture between M. athalia and M. celadussa at the contact zone, though not reaching the Balkan clade. The demographic modelling of populations supported the intermediate genetic make-up of European M. athalia populations with regards to M. celadussa and the Balkan clade. However, the dissimilarity matrix of genotype data (PCoA) suggested the Balkan lineage having a genetic component that is unrelated to the athalia-celadussa group. Although narrowly sympatric, almost no signs of gene flow were found between the main M. athalia group and the Balkan clade. We propose two possible scenarios on the historical evolution of our model taxa and the role of the last glacial maximum in shaping their current distribution. Finally, we discuss the complexities regarding the taxonomic delimitation of parapatric taxa.

Highlights

Difficulties to delimit species under many circumstances are severely undermining attempts to catalogue global biodiversity and have an adverse effect on conservation efforts [1]
The neighbor joining (NJ) tree based on DNA barcodes (Figure S1) grouped specimens of M. athalia–M. celadussa into three main well-supported (Bootstrap Support (BS) > 0.95) clusters
Based on their established distribution [22], one cluster was assigned to M. celadussa, and the other two to M. athalia

Summary

Introduction

Difficulties to delimit species under many circumstances are severely undermining attempts to catalogue global biodiversity and have an adverse effect on conservation efforts [1]. These difficulties stem from both biological and operational causes. Ontological difficulties, in turn, are largely due to the lack of consensus over the species concept and critical properties that a population should bear in order to be considered as a valid species [3]. Insect species have largely been circumscribed based on morphological traits, assuming that morphological differences, those in genitalia, play a key role in preventing gene flow between populations undergoing speciation [5]. The “lockand-key hypothesis”, i.e., an idea that genital differences between species have evolved in order to prevent insemination across species [6], was long popular among entomologists, it suffers from both theoretical weaknesses [7,8] and a lack of empirical support [2,9,10]

Objectives

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Conclusion