Relaxed selection underlies genome erosion in socially parasitic ant species

Lukas Schrader,Morten Schiøtt,Fredrick J Larabee,Christian Rabeling,Jacobus J Boomsma,Guojie Zhang,Yuan Deng,Xupeng Bi,Hailin Pan,Martin Bollazzi

doi:10.1038/s41467-021-23178-w

Abstract

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. They have evolved many times convergently, are often evolutionarily young lineages, and are almost invariably rare. Focusing on the leaf-cutting ant genus Acromyrmex, we compared genomes of three inquiline social parasites with their free-living, closely-related hosts. The social parasite genomes show distinct signatures of erosion compared to the host lineages, as a consequence of relaxed selective constraints on traits associated with cooperative ant colony life and of inquilines having very small effective population sizes. We find parallel gene losses, particularly in olfactory receptors, consistent with inquiline species having highly reduced social behavioral repertoires. Many of the genomic changes that we uncover resemble those observed in the genomes of obligate non-social parasites and intracellular endosymbionts that branched off into highly specialized, host-dependent niches.

Highlights

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species
To identify genetic changes associated with the shift from cooperative social colony life to social parasitism, we de novo sequenced genomes of four Acromyrmex species, including the three inquiline social parasites A. charruanus, A. insinuator, and Pseudoatta argentina, as well as A. heyeri, the host species of A. charruanus and P. argentina
Using microCT scans, we explored whether the relative size of the olfactory lobes (OL) was smaller in inquiline social parasite species compared to their hosts, mirroring the reduced olfactory receptors (ORs) repertoire encoded in their genomes

Summary

Introduction

Inquiline ants are highly specialized and obligate social parasites that infiltrate and exploit colonies of closely related species. Evolutionary transitions in bacteria from a free-living to an endosymbiotic lifestyle are almost invariably associated with convergent phenotypic and genomic reductions[21] In many of these cases, changes in effective population sizes (Ne) due to permanent asexual reproduction or frequent bottlenecks reduce the efficacy of selection. Analogous to intracellular and specialized non-social parasites, the evolution of inquilines has classically been described as a degenerative process[29,30] almost invariably converging on a similar suite of morphological and behavioral characteristics across independently evolved inquilines[31] This so-called “social parasite syndrome” subsumes an array of regressive phenotypic changes, such as the reduction or complete loss of the worker caste, simplified mouthparts, antennae and integuments, loss of certain exocrine glands, and a nervous system of reduced complexity likely associated with a drastically narrowed behavioral repertoire[27,28,29,30,32,33].

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Conclusion