Phylogeography of social polymorphism in a boreo-montane ant

Abstract

BackgroundThe disjunct distribution of several Palearctic species has been widely shaped by the changes in climatic conditions during the Quaternary. The observed genetic differentiation or reproductive isolation between extant populations may be the outcome of their contemporary geographic separation or reproductive incompatibility due to differences in phenotypic traits which have evolved in isolated refugia. In the boreal ant Leptothorax acervorum, colonies from central and peripheral populations differ in social structure: colonies from Central and Northern Europe may contain several equally reproductive queens (facultative polygyny), while in colonies from peripheral populations in Spain only one the most dominant of several queens lays eggs (functional monogyny). By reconstructing the specie’s evolutionary and demographic history in Southwestern Europe we examine whether variation in social organization is associated with restricted gene flow between the two social forms.ResultsWe show that multi-queen colonies from all so far known inner Iberian populations of L. acervorum are functionally monogynous, whereas multi-queen colonies from all Pyrenean populations are polygynous, like those from other previously studied areas in Europe. Our analyses revealed complex spatial-genetic structure, but no association between spatial-genetic structure and social organization in SW-Europe. The population in the western Pyrenees diverged most strongly from other Iberian populations. Moreover, microsatellite data suggest the occurrence of recent bottlenecks in Pyrenean and inner Iberian populations.ConclusionsOur study shows a lack of reproductive isolation between the two social forms in SW-Europe. This in turn suggests that demographic and spatial patterns in genetic variation as well as the distribution of social phenotypes are better explained by co-variation with climatic, ecological, and historical factors. Moreover, we for the first time show the existence of substantial spatial-genetic structure in L. acervorum, suggesting the existence of multiple refugia in SW-Europe, including two extra-Mediterranean refugia in France. While gene flow among inner Iberian refugia may have been larger during the late glacial, extra-Mediterranean refugia in southern France may have contributed to the post-glacial recolonization of W-Europe.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0711-3) contains supplementary material, which is available to authorized users.

Phylogeny of theFormicoxenusgenus-group (Hymenoptera: Formicidae) reveals isolated lineages ofLeptothorax acervorumin the Iberian Peninsula predating the Last Glacial Maximum

“…Our results indicate that all populations we included within the IP, except Larra and Pla de la Font, seem to have been more isolated from the remaining range of distribution of this species (Fig. 4), supporting previous evidence based on SSRs, which have found evidence of bottlenecks and varying levels of connectivity in this area (Trettin et al, 2016). However, there are only a few mutations separating even the most divergent haplotypes among these populations, but these divergent haplotypes in the IP tend to be found in altitudinally restricted populations.…”

“…A de novo mitochondrial genome was identified as part of a whole genome sequencing project from a single adult male (PF population, sample: PF18_15_M1) using 10x linked reads assembled with Supernova 2.1.1 (Weisenfeld et al, 2018). The scaffold containing the mtDNA genome was identified by a BLASTn query of the assembled genome with two published L. acervorum mtDNA sequences (query 1: COXI -tRNA -Leu -COXII: GenBank: KU245569 (Trettin et al, 2016); query 2: COB: GenBank: HQ259995 (Gill et al, 2009). These two sequences, located ~6Kb apart in the canonical hymenopteran mtDNA genome, were used to minimize erroneous matches to nuclear genomic scaffolds containing translocated mtDNA (NUMTs).…”

“…Previous phylogeographic analyses within L. acervorum species have been based on the COI 3'P region and indicate substantial genetic diversity within the species (Brandt et al, 2007;Foitzik et al, 2009;Trettin et al, 2016). The most recent analyses based on SSRs and mtDNA (COI 3'P region) have found the existence of multiple refugia in SW-Europe, and evidence of spatial genetic structure across the sampled area (Trettin et al, 2016). Our most extensive data set, including specimens we identified in the previous phylogenetic analyses (Fig.…”

“…Leptothorax acervorum is one of the only three ant species with Holarctic distribution (Schär et al, 2018); however, all current phylogeographic analyses of this species based on alloenzymes, SSRs, mtDNA and nuclear markers have included only Palearctic specimens (Brandt et al, 2007;Foitzik et al, 2009;Gill et al, 2009;Stille and Stille, 1993;Trettin et al, 2016), thus providing an incomplete picture of the patterns of recolonization and populations structure. Previous phylogeographic analyses within L. acervorum species have been based on the COI 3'P region and indicate substantial genetic diversity within the species (Brandt et al, 2007;Foitzik et al, 2009;Trettin et al, 2016). The most recent analyses based on SSRs and mtDNA (COI 3'P region) have found the existence of multiple refugia in SW-Europe, and evidence of spatial genetic structure across the sampled area (Trettin et al, 2016).…”

“…These analyses have found generally less population structure in L. acervorum compared to other species closely related species within Leptothorax, e.g. L. muscorum (Nylander, 1846) and Harpagoxenus sublaevis (Nylander, 1849) (Brandt et al, 2007;Foitzik et al, 2009;Trettin et al, 2016), but also evidence of divergent haplotypes have been found in the Pyrenees and Southern France (Trettin et al, 2016). Given the large distribution range across the Holarctic and the extensive variation in the latitudinal range in western Europe (from the Iberian Peninsula to North Cape in Norway) (Heinze and Holldobler, 1994), approaches that combine analyses at different taxonomic levels with extensive sampling are necessary to understand the phylogenetic relationships and evolutionary history of Leptothorax species.…”