Genetic and chemical divergence among host races of a socially parasitic ant.

Candice W Torres,Neil D Tsutsui,Santiago R Ramírez,Maria A Tonione,Joseph R Sapp

doi:10.1002/ece3.4547

Abstract

Host–parasite associations facilitate the action of reciprocal selection and can drive rapid evolutionary change. When multiple host species are available to a single parasite, parallel specialization on different hosts may promote the action of diversifying natural selection and divergence via host race formation. Here, we examine a population of the kidnapper ant (Polyergus mexicanus) that is an obligate social parasite of three sympatric ant species: Formica accreta, F. argentea, and F. subaenescens (formerly F. fusca). Behavioral and ecological observations of P. mexicanus have shown that individual colonies parasitize only one species of host and that new Polyergus queens maintain host fidelity when establishing new colonies. To successfully adapt to a particular host, Polyergus ants may mimic or camouflage themselves with the species‐specific chemical cues (cuticular hydrocarbons) that their hosts use to ascertain colony membership. To investigate the extent of host specialization, we collected both genetic and chemical data from P. mexicanus that parasitize each of the three different Formica species in sympatry. We show that host‐associated genetic structure exists for both maternally inherited mitochondrial DNA data and biparentally inherited microsatellite markers. We also show that P. mexicanus can be distinguished by chemical profile according to host due to partial matching with their host. Our results support the hypothesis that host race formation is occurring among lineages of P. mexicanus that use different Formica hosts. Thus, this system may represent a promising model for illuminating the early steps of divergence, accumulation of reproductive isolation, and speciation.

Highlights

Divergent natural selection imposed by environmental gradients drives local adaptation, increases genetic and phenotypic differ‐ entiation, and can lead to reproductive isolation
A special case of adaptation leading to differentiation occurs when populations form host races, as when herbivores become adapted to different food plants (Forbes et al, 2017; Walsch, 1864) or when lineages of para‐ sites become adapted to different hosts (Nosil, 2012; Nosil, Harmon, & Seehausen, 2009; Via, 2009)
We test the hypothesis that these Polyergus lineages dis‐ play significant phenotypic differentiation from each other in the pheromones used for colony recognition. We address this hypothesis by extracting cuticular hydrocarbons from field‐collected ants and analyzing them using gas chromatogra‐ phy–mass spectrometry (GC‐Mass Spectrometer (MS))

Summary

Introduction

Divergent natural selection imposed by environmental gradients drives local adaptation, increases genetic and phenotypic differ‐ entiation, and can lead to reproductive isolation. We examine the molecular and chemical ecology of the socially parasitic kidnapper ant, P. mexicanus (formerly P. breviceps), which parasitizes three sympatric species of Formica at our study site: F. accreta, F. argentea, and F. subaenescens.

Results

Conclusion