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

Abstract

Understanding the dynamics of biodiversity, including the spatial distribution of genetic diversity, is critical for predicting responses to environmental changes, as well as for effective conservation measures. This task requires tracking changes in biodiversity at large spatial scales and correlating with species functional traits. We provide three comprehensive resources to understand the determinants for mitochondrial DNA differentiation represented by (a) 15,609 COI sequences and (b) 14 traits belonging to 307 butterfly species occurring in Western‐Central Europe and (c) the first multi‐locus phylogenetic tree of all European butterfly species. By applying phylogenetic regressions we show that mitochondrial DNA spatial differentiation (as measured with GST, G′ST, D and DST) is negatively correlated with species traits determining dispersal capability and colonization ability. Thanks to the high spatial resolution of the COI data, we also provide the first zoogeographic regionalization maps based on intraspecific genetic variation. The overall pattern obtained by averaging the spatial differentiation of all Western‐Central European butterflies shows that the paradigm of long‐term glacial isolation followed by rapid pulses of post‐glacial expansion has been a pervasive phenomenon in European butterflies. The results and the extensive data sets we provide here constitute the basis for genetically‐informed conservation plans for a charismatic group in a continent where flying insects are under alarming decline.

Next generation sequencing-aided comprehensive geographic coverage sheds light on the status of rare and extinct populations of Aporia butterflies (Lepidoptera: Pieridae)

“…karavaievi, and ssp. rutae respectively) recognized by Della Bruna et al 9 , confirming a pervasive phylogeographic pattern in European phylogeography 50,51 . The trace of demographic expansion model indeed dates a rapid expansion of the Mediterranean haplogroup to about 116 kya during the Late Pleistocene.…”

“…Conversely, the Greek populations did not expand to Central Europe despite the absence of conspicuous mountain chains that would otherwise impede such colonization. Although the validity of using mtDNA as a marker in molecular ecology has been questioned in the last decade 56,57 , a recent study has provided evidence that mtDNA spatial differentiation is correlated with species traits known to affect the dispersal and colonization capabilities of butterflies 51 . Nevertheless, considering that the mtDNA variation observed in this study is not representative of the whole genomic variation, we cannot exclude a recent expansion of the Greek populations in Central Europe.…”

How long is 3 km for a butterfly? Ecological constraints and functional traits explain high mitochondrial genetic diversity between Sicily and the Italian Peninsula

“…Comparative studies indicate that different species attributes (e.g. population size, fecundity, body size, dispersal capability) explain mtDNA polymorphism and its spatial differentiation (Allio et al, 2017; Burney & Brumfield, 2009; Dapporto et al, 2017, 2019; Fujisawa et al, 2015; Nabholz et al, 2008). Adult is the most mobile life stage in butterflies and the length of the flight period largely determines the potential dispersal events and the consequent gene flow.…”

“…We tested the existence of a phylogenetic signal for species traits with Pagel's lambda index by applying the phylosig function of the phytools r package. As a reference phylogeny, we used the recently published phylogenetic tree based on 14 genes (1 mitochondrial and 13 nuclear) of all European butterflies (Dapporto et al, 2019).…”

“…This approach may disentangle the role played by deterministic processes with respect to stochasticity in structuring the spatial genetic variation and shed light on the historical/contemporary and biotic/abiotic processes that enabled the establishment and maintenance of the observed phylogeographic patterns. Comparative phylogeography has been facilitated by advancements in DNA sequencing and the availability of large genetic datasets in public repositories (GenBank and BOLD; Burney & Brumfield, 2009; Dapporto et al, 2017, 2019; Fujisawa, Vogler, & Barraclough, 2015; Moritz et al, 2009; Pigot & Tobias, 2014), mostly in the form of mitochondrial DNA (mtDNA) cytochrome c oxidase subunit 1 (COI) sequences. The particularly fast mutation rate and the short coalescence time characterizing mtDNA produce frequent cases of genetic differentiation among allopatric populations (Allio, Donega, Galtier, & Nabholz, 2017), thus making mtDNA a widely used marker in phylogeography (Avise, 2000).…”