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

Abstract

We present a phylogeographic study of at least six reproductively isolated lineages of new world harvester ants within the Pogonomyrmex barbatus and P. rugosus species group. The genetic and geographic relationships within this clade are complex: Four of the identified lineages show genetic caste determination (GCD) and are divided into two pairs. Each pair has evolved under a mutualistic system that necessitates sympatry. These paired lineages are dependent upon one another because their GCD requires interlineage matings for the production of F1 hybrid workers, and intralineage matings are required to produce queens. This GCD system maintains genetic isolation among these interdependent lineages, while simultaneously requiring co-expansion and emigration as their distributions have changed over time. It has also been demonstrated that three of these four GCD lineages have undergone historical hybridization, but the narrower sampling range of previous studies has left questions on the hybrid parentage, breadth, and age of these groups. Thus, reconstructing the phylogenetic and geographic history of this group allows us to evaluate past insights and hypotheses and to plan future inquiries in a more complete historical biogeographic context. Using mitochondrial DNA sequences sampled across most of the morphospecies’ ranges in the U.S.A. and Mexico, we conducted a detailed phylogeographic study. Remarkably, our results indicate that one of the GCD lineage pairs has experienced a dramatic range expansion, despite the genetic load and fitness costs of the GCD system. Our analyses also reveal a complex pattern of vicariance and dispersal in Pogonomyrmex harvester ants that is largely concordant with models of late Miocene, Pliocene, and Pleistocene range shifts among various arid-adapted taxa in North America.

Comparative phylogeography clarifies the complexity and problems of continental distribution that drove A. R. Wallace to favor islands

“…2). Reinforcing this observation within the same system, one recent study (48) used the backbone general phylogeographic pattern to gain understanding into the historical development of a complex life history structure between two species of ants in the genus Pogonomyrmex. Another (49) took advantage of combining mtDNA and ddRADseq SNPs to reveal both a deep phylogeographic break (mtDNA) and recent gene flow (SNPs) across a transition zone that is coincident with at least 14 additional cryptic taxon pairs of mammals, birds, and herps (19,44), suggesting the prospect of studying ongoing speciation processes across a transition zone (that almost certainly contains a rich history of temporal pseudocongruence) at a community scale using similar genomic tools, dramatically building on Remington's (11) concept of suture zones.…”

Methylation and gene expression differences between reproductive and sterile bumblebee workers

“…The mechanisms by which species develop differences between castes are diverse; some species use only environmental cues, whereas others rely only on inherited changes, with many species falling somewhere in between these two extremes (Matsuura et al 2018). For example, some ant species from the Pogonomyrmex genus have purely genetic caste determination (Mott et al 2015). On the other hand, many ant species undergo caste determination in response to only the environment, indicating their genomes must contain the code for all caste possibilities, with the phenotype potentially determined by epigenetic factors (Bonasio et al 2012).…”

“…For example, some ant species from the Pogonomyrmex genus have purely genetic caste determination (Mott et al. ). On the other hand, many ant species undergo caste determination in response to only the environment, indicating their genomes must contain the code for all caste possibilities, with the phenotype potentially determined by epigenetic factors (Bonasio et al.…”

Two lineages that need each other

“…; Mott et al . ). It seems that there may have been hybridization in the past, but not in the present, and that even within populations, different systems for producing workers and reproductives may be at work.…”

“…'Hybridogenesis' in ants sometimes refers to the hypothesis that the dependent-lineage system is the result of hybridization between related sympatric species. This hypothesis for Pogonomyrmex harvester ants is controversial and has not been supported by phylogenetic evidence (Anderson et al 2008;Sirvi€ o et al 2011;Mott et al 2015). It seems that there may have been hybridization in the past, but not in the present, and that even within populations, different systems for producing workers and reproductives may be at work.…”