Widespread hybridization within mound‐building wood ants in Southern Finland results in cytonuclear mismatches and potential for sex‐specific hybrid breakdown

Abstract

Hybridization and gene flow between diverging lineages are increasingly recognized as common evolutionary processes, and their consequences can vary from hybrid breakdown to adaptive introgression. We have previously found a population of wood ant hybrids between Formica aquilonia and F. polyctena that shows antagonistic effects of hybridization: females with introgressed alleles show hybrid vigour, whereas males with the same alleles show hybrid breakdown. Here, we investigate whether hybridization is a general phenomenon in this species pair and analyse 647 worker samples from 16 localities in Finland using microsatellite markers and a 1200-bp mitochondrial sequence. Our results show that 27 sampled nests contained parental-like gene pools (six putative F. polyctena and 21 putative F. aquilonia) and all remaining nests (69), from nine localities, contained hybrids of varying degrees. Patterns of genetic variation suggest these hybrids arise from several hybridization events or, instead, have backcrossed to the parental gene pools to varying extents. In contrast to expectations, the mitochondrial haplotypes of the parental species were not randomly distributed among the hybrids. Instead, nests that were closer to parental-like F. aquilonia for nuclear markers preferentially had F. polyctena's mitochondria and vice versa. This systematic pattern suggests there may be underlying selection favouring cytonuclear mismatch and hybridization. We also found a new hybrid locality with strong genetic differences between the sexes similar to those predicted under antagonistic selection on male and female hybrids. Further studies are needed to determine the selective forces that act on male and female genomes in these newly discovered hybrids.

Temperature fluctuations between years predict temporal allele frequency variation in a hybrid ant population

“…Hybridization can occur between differentially temperature-adapted species (Pereira et al 2016), which can lead to changes in temperature tolerance (Pereira et al 2014) and the colonization of novel habitats (Gompert et al 2006). Albeit sparse, genetic data suggests pure F. polyctena populations are in minority in Finland (Beresford et al 2017), and hybridization could have allowed them to colonize this far North in the first place (e.g. Krehenwinkel and Tautz 2013).…”

“…Currently, Formica polyctena has a more southern range while F. aquilonia has a boreo-alpine range (Fig. 1) (Stockan and Robinson 2016), but their distributions overlap in Southern Finland where multiple hybrid populations occur (Beresford et al 2017). In this region, the Långholmen population encompasses more than 25 ant nests and is the most extensively studied hybrid population.…”

“…In this region, the Långholmen population encompasses more than 25 ant nests and is the most extensively studied hybrid population. Previous studies indicating the coexistence of two distinct genetic lineages named F. polyctena -like (formerly named R) and F. aquilonia -like (formerly named W) (Beresford et al 2017; Kulmuni et al 2019; Kulmuni and Pamilo 2014; Kulmuni et al 2010). Both lineages are hybrids but currently inhabit different nests within the population (Kulmuni et al 2010).…”

Evidence for natural selection and barrier leakage in candidate loci underlying speciation in wood ants

“…The age of the hybrid population is unknown, but present-day individuals are not first-generation hybrids. Instead, the study population divides into two genetic lineages in a very similar way to the swordtail fish [14]; within the hybrid population one lineage is genetically more similar to one of the parental species, Formica aquilonia (previously referred to as W group), and the other is closer to the other parental species, F. polyctena (previously referred to as R group) [15]. Even though both lineages are of hybrid origin they show signs of reproductive isolation, as 94.5 % of successful matings are within a lineage [11,12] and we have never observed reproductive adult F1 individuals in nature.…”

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

“…The fitness landscape described here (Figure ) is inspired by the situation observed in Finnish Formica ants (Beresford et al., ; Kulmuni & Pamilo, ; Kulmuni et al., ). There, the authors discovered heterosis in the diploid females but recessive incompatibilities expressed in the haploid males.…”