An official website of the United States government
Abstract Social parasites exploit the brood care behavior of their hosts to raise their own offspring. Social parasites are common among eusocial Hymenoptera and exhibit a wide range of distinct life history traits in ants, bees, and wasps. In ants, obligate inquiline social parasites are workerless (or nearly-so) species that engage in lifelong interactions with their hosts, taking advantage of the existing host worker forces to reproduce and exploit host colonies’ resources. Inquiline social parasites are phylogenetically diverse with approximately 100 known species that evolved at least 40 times independently in ants. Importantly, ant inquilines tend to be closely related to their hosts, an observation referred to as ‘Emery’s Rule’. Polygyny, the presence of multiple egg-laying queens, was repeatedly suggested to be associated with the origin of inquiline social parasitism, either by providing the opportunity for reproductive cheating, thereby facilitating the origin of social parasite species, and/or by making polygynous species more vulnerable to social parasitism via the acceptance of additional egg-laying queens in their colonies. Although the association between host polygyny and the evolution of social parasitism has been repeatedly discussed in the literature, it has not been statistically tested in a phylogenetic framework across the ants. Here, we conduct a meta-analysis of ant social structure and social parasitism, testing for an association between polygyny and inquiline social parasitism with a phylogenetic correction for independent evolutionary events. We find an imperfect but significant over-representation of polygynous species among hosts of inquiline social parasites, suggesting that while polygyny is not required for the maintenance of inquiline social parasitism, it (or factors associated with it) may favor the origin of socially parasitic behavior. Our results are consistent with an intra-specific origin model for the evolution of inquiline social parasites by sympatric speciation but cannot exclude the alternative, inter-specific allopatric speciation model. The diversity of social parasite behaviors and host colony structures further supports the notion that inquiline social parasites evolved in parallel across unrelated ant genera in the formicoid clade via independent evolutionary pathways.
more »
« less
Relaxed selection underlies genome erosion in socially parasitic ant species
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.
more »
« less
- Award ID(s):
- 1654829
- PAR ID:
- 10309979
- Date Published:
- Journal Name:
- Nature Communications
- Volume:
- 12
- Issue:
- 1
- ISSN:
- 2041-1723
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Aim One of the most consistent global biogeographic patterns is the latitudinal diversity gradient where species richness peaks within the equatorial tropics and decreases towards the poles. Here, we explore the global biogeography of socially parasitic ant species, which comprises the most diverse group of social parasites in the Hymenoptera. We test the biogeographic hypothesis that ant social parasites are distributed along an inverse latitudinal diversity gradient (iLDG) by peaking in diversity outside of the equatorial tropics, which would contrast with the biogeographic pattern observed in free-living, non-parasitic ant species. Location Global. Taxon Ants (Hymenoptera: Formicidae). Methods We assembled a comprehensive biogeographic dataset consisting of 6001 geographic distribution records for all 371 taxonomically described socially parasitic ant species. We used phylogenetic and taxonomic studies to estimate the number of independent evolutionary origins of ant social parasitism to directly compare species richness with the number of species representing independent evolutionary origins of social parasitism across a latitudinal gradient. In addition, we compared ant social parasite diversity across biogeographic regions using rarefaction to account for different sampling efforts. Finally, we tested for a correlation between latitude and the proportion of ant social parasite species within regional ant faunae. Results The geographic distribution records and the inferred 91 independent evolutionary origins of socially parasitic life histories in ants show that both species richness and the number of species representing independent evolutionary origins of social parasitism peak in the northern hemisphere outside of the equatorial tropics. Based on rarefaction curves, northern latitude regions harbour the most ant social parasite species, but the diversity of independent evolutionary origins is not significantly different between northern and southern hemispheres. The proportion of ant social parasite species within regional faunae is tightly correlated with latitude only in the northern hemisphere. Main conclusions The iLDG of ant social parasites contrasts with the biogeographic pattern observed in free-living, non-parasitic ant species and appears to be driven by large species radiations as well as by the presence of specialized life histories exclusive to the northern hemisphere.more » « less
-
Abstract Ant nests are biodiversity hot spots, concentrating resources from a wide area that can be exploited by other organisms, known as myrmecophiles. The mite order Mesostigmata includes a wide range of lineages that have become myrmecophiles with many species reliant on ant nests for at least part of their development. The nature of the associations is quite variable, including predators of smaller arthropods in the nest (close to the ancestral lifestyle of these mites), scavengers, kleptoparasites, parasites, and parasitoids. A few mite species show extreme modifications of morphological and/or developmental patterns, others show almost none. Some host specificity is common but one-on-one host specialization is rare or poorly tested. Phoresy on the ants is common, but the target ant caste varies with the goal of phoresy. In general, the diversity of mesostigmatid mites in the nest of a given ant species is affected by habitat conditions along with a range of life history characteristics of the ants, including factors such as body size, colony size, colony founding mode, social parasitism, and nest density. Unfortunately, the life history of the majority of mites associated with ants is still unknown.more » « less
-
The metabolic intimacy of symbiosis often demands the work of specialists. Natural products and defensive secondary metabolites can drive specificity by ensuring infection and propagation across host generations. But in contrast to bacteria, little is known about the diversity and distribution of natural product biosynthetic pathways among fungi and how they evolve to facilitate symbiosis and adaptation to their host environment. In this study, we define the secondary metabolism of Escovopsis and closely related genera, symbionts in the gardens of fungus-farming ants. We ask how the gain and loss of various biosynthetic pathways correspond to divergent lifestyles. Long-read sequencing allowed us to define the chromosomal features of representative Escovopsis strains, revealing highly reduced genomes composed of seven to eight chromosomes. The genomes are highly syntenic with macrosynteny decreasing with increasing phylogenetic distance, while maintaining a high degree of mesosynteny. An ancestral state reconstruction analysis of biosynthetic pathways revealed that, while many secondary metabolites are shared with non-ant-associated Sordariomycetes, 56 pathways are unique to the symbiotic genera. Reflecting adaptation to diverging ant agricultural systems, we observe that the stepwise acquisition of these pathways mirrors the ecological radiations of attine ants and the dynamic recruitment and replacement of their fungal cultivars. As different clades encode characteristic combinations of biosynthetic gene clusters, these delineating profiles provide important insights into the possible mechanisms underlying specificity between these symbionts and their fungal hosts. Collectively, our findings shed light on the evolutionary dynamic nature of secondary metabolism in Escovopsis and its allies, reflecting adaptation of the symbionts to an ancient agricultural system.Microbial symbionts interact with their hosts and competitors through a remarkable array of secondary metabolites and natural products. Here, we highlight the highly streamlined genomic features of attine-associated fungal symbionts. The genomes of Escovopsis species, as well as species from other symbiont genera, many of which are common with the gardens of fungus-growing ants, are defined by seven chromosomes. Despite a high degree of metabolic conservation, we observe some variation in the symbionts’ potential to produce secondary metabolites. As the phylogenetic distribution of the encoding biosynthetic gene clusters coincides with attine transitions in agricultural systems, we highlight the likely role of these metabolites in mediating adaptation by a group of highly specialized symbionts.more » « less
-
Abstract Biparental sex is widespread in nature, yet costly relative to uniparental reproduction. It is generally unclear why self-fertilizing or asexual lineages do not readily invade outcrossing populations. The Red Queen hypothesis predicts that coevolving parasites can prevent self-fertilizing or asexual lineages from invading outcrossing host populations. However, only highly virulent parasites are predicted to maintain outcrossing, which may limit the general applicability of the Red Queen hypothesis. Here, we tested whether the ability of coevolving parasites to prevent invasion of self-fertilization within outcrossing host populations was dependent on parasite virulence. We introduced wild-type Caenorhabditis elegans hermaphrodites, capable of both self-fertilization and outcrossing, into C. elegans populations fixed for a mutant allele conferring obligate outcrossing. Replicate C. elegans populations were exposed for 24 host generations to one of four strains of Serratia marcescens parasites that varied in virulence, under three treatments: a heat-killed (control, noninfectious) parasite treatment, a fixed-genotype (nonevolving) parasite treatment, and a copassaged (potentially coevolving) parasite treatment. As predicted, self-fertilization invaded C. elegans host populations in the control and fixed-parasite treatments, regardless of parasite virulence. In the copassaged treatment, selfing invaded host populations coevolving with low- to mid-virulence strains, but remained rare in hosts coevolving with highly virulent bacterial strains. Therefore, we found that only highly virulent coevolving parasites can impede the invasion of selfing.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1038/s41467-021-23178-w
