The Potential for Gene Flow in a Dependent Lineage System of a Harvester Ant: Fair Meiosis in the F1 Generation

Abstract

We investigated the potential for gene flow in a dependent lineage (DL) system of the harvester ant Pogonomyrmex. Each DL system is composed of 2 reproductively isolated lineages that are locked in an obligate mutualism. The genetic components that produce the worker phenotype are acquired by hybridizing with the partner lineage. In the mating flight, queens of both lineages mate with multiple males from each lineage. During colony growth and reproduction, eggs fertilized by partner-lineage sperm produce F(1) hybrid workers with interlineage genomes, whereas eggs fertilized by same-lineage sperm result in the development of new queens with intralineage genomes. New males are typically produced from unfertilized eggs laid by the pure-lineage queen but in her absence may be produced by interlineage F(1) workers. We investigated the potential for interlineage gene flow in this system using 2 classes of lineage-specific nuclear markers to identify hybrid genome combinations. We confirmed the production of viable interlineage F(1) reproductive females in field colonies, the occurrence of which is associated with the relative frequencies of each lineage in the population: interlineage F(1) queens occurred only in the rare lineage of the population with dramatically skewed lineage frequencies. In laboratory colonies, we detected fair meiosis in interlineage F(1) workers leading to the production of viable and haploid interlineage F(2) males. We conclude that the genomes of each lineage recombine freely, suggesting that extrinsic postzygotic selection maintains the integrity of each lineage genome. We compare our findings with those of the H1/H2 DL system.

Phylogeography ofPogonomyrmex barbatusandP. rugosusharvester ants with genetic and environmental caste determination

“…Fortunately, three previous studies have confirmed that the GCD phenotype maps onto just two discrete and apparently monophyletic clades in mtDNA phylogenies constructed from cox1 sequences (Helms Cahan and Keller 2003;Anderson et al 2006;Schwander et al 2007a). Moreover, these and other studies have repeatedly found that J and H lineages are reproductively isolated from each other and from ECD P. barbatus and P. rugosus (Helms Cahan and Keller 2003;Anderson et al 2006;Helms Cahan et al 2006;Schwander et al 2007aSchwander et al , 2007bCurry et al 2010;Sirvi€ o et al 2010). To the extent that this pattern is maintained across a broader geographic range, it is possible to define samples as derived from either a GCD or ECD clade based on phylogenetic analyses.…”

“…; Curry et al. ; Sirviö et al ). To the extent that this pattern is maintained across a broader geographic range, it is possible to define samples as derived from either a GCD or ECD clade based on phylogenetic analyses.…”

Introgression of mitochondrial DNA among lineages in a hybridogenetic ant

“…Such males could father new hybrid queens, a situation that may lead ultimately to offspring with introgressed mitochondria. Both hybrid queens and hybrid males occur in Pogonomyrmex ants [18]. Nevertheless, interlineage hybrid queens of Pogonomyrmex are known to have reduced fitness, if any [17].…”

Convergent evolution of social hybridogenesis in Messor harvester ants

“…Queens that only mate with males of different lineage fail to produce new queens, while queens that only mate with males of their own lineage fail to produce workers and the colony is therefore not viable. Understanding the origin and maintenance of this unique system requiring three different mating partners has attracted considerable interest (Anderson et al 2006(Anderson et al , 2008Linksvayer et al 2006;Schwander et al 2006Schwander et al , 2007aVolny et al 2006;Yamauchi & Yamamura 2006;Curry et al 2009;Sirvi€ o et al 2010;Suni & Gordon 2010;Gordon et al 2013;Mott et al 2015). However, no new cases have been found since its discovery (Julian et al 2002).…”