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Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants.Acromyrmexleaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South AmericanAcromyrmexspecies to study how different selective pressures influence the evolution of polygyny and polyandry. We show thatAcromyrmexspecies exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species,Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species,A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution inAcromyrmexleaf-cutting ants.

Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

 

Nylanderia(Emery) is one of the world's most diverse ant genera, with 123 described species worldwide and hundreds more undescribed. Fifteen globetrotting or invasive species have widespread distributions and are often encountered outside their native ranges. A molecular approach to understanding the evolutionary history and to revision ofNylanderiataxonomy is needed because historical efforts based on morphology have proven insufficient to define major lineages and delimit species boundaries, especially where adventive species are concerned. To address these problems, we generated the first genus‐wide genomic dataset ofNylanderiausing ultraconserved elements (UCEs) to resolve the phylogeny of major lineages, determine the age and origin of the genus, and describe global biogeographical patterns. Sampling from seven biogeographical regions revealed a Southeast Asian origin ofNylanderiain the mid‐Eocene and four distinct biogeographical clades in the Nearctic, the Neotropics, the Afrotropics/Malagasy region, and Australasia. The Nearctic and Neotropical clades are distantly related, indicating two separate dispersal events to the Americas between the late Oligocene and early Miocene. We also addressed the problem of misidentification that has characterized species‐level taxonomy inNylanderiaas a result of limited morphological variation in the worker caste by evaluating the integrity of species boundaries in six of the most widespreadNylanderiaspecies. We sampled across ranges of species in theN. bourbonicacomplex (N. bourbonica(Forel) + N. vaga(Forel)), theN. fulvacomplex (N. fulva(Mayr) + N. pubens(Forel)), and theN. guatemalensiscomplex (N. guatemalensis(Forel) + N. steinheili(Forel)) to clarify their phylogenetic placement. Deep splits within these complexes suggest that some species names – specificallyN. bourbonicaandN. guatemalensis– each are applied to multiple cryptic species. In exhaustively samplingNylanderiadiversity in the West Indies, a ‘hot spot’ for invasive taxa, we found five adventive species among 22 in the region; many remain morphologically indistinguishable from one another, despite being distantly related. We stress that overcoming the taxonomic impediment through the use of molecular phylogeny and revisionary study is essential for conservation and invasive species management.

 

Fungus‐farming ants (Hymenoptera: Formicidae) have become model systems for exploring questions regarding the evolution of symbiosis. However, robust phylogenetic studies of both the ant agriculturalists and their fungal cultivars are necessary for addressing whether or not observed ant–fungus associations are the result of coevolution and, if so, whether that coevolution has been strict or diffuse. Here we focus on the evolutionary relationships of the species within the ant genusMyrmicocryptaand of their fungal cultivars. The fungus‐farming ant genusMyrmicocryptawas created by Fr. Smith in 1860 based on a single alate queen. Since then, 31 species and subspecies have been described. Until now, the genus has not received any taxonomic treatment and the relationships of the species within the genus have not been tested. Our molecular analyses, using ∼40 putative species and six protein‐coding (nuclear and mitochondrial) gene fragments, recoverMyrmicocryptaas monophyletic and as the sister group of the genusMycocepurusForel. The speciesM. tuberculataWeber is recovered as the sister to the rest ofMyrmicocrypta. The time‐calibrated phylogeny recovers the age of stem groupMyrmicocryptaplus its sister group as 45 Ma, whereas the inferred age for the crown groupMyrmicocryptais recovered as 27 Ma. Ancestral character‐state analyses suggest that the ancestor ofMyrmicocryptahad scale‐like or squamate hairs and that, although such hairs were once considered diagnostic for the genus, the alternative state of erect simple hairs has evolved at least seven independent times. Ancestral‐state analyses of observed fungal cultivar associations suggest that the most recent common ancestor ofMyrmicocryptacultivated clade 2 fungal species and that switches to clade 1 fungi have occurred at least five times. It is our hope that these results will encourage additional species‐level phylogenies of fungus‐farming ants and their fungal cultivars, which are necessary for understanding the evolutionary processes that gave rise to agriculture in ants and that produced the current diversity of mutualistic ant–fungus interactions.

 

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. 

Studying the behavioral and life history transitions from a cooperative, eusocial life history to exploitative social parasitism allows for deciphering the conditions under which changes in behavior and social organization lead to diversification. The Holarctic ant genus Formica is ideally suited for studying the evolution of social parasitism because half of its 172 species are confirmed or suspected social parasites, which includes all three major classes of social parasitism known in ants. However, the life history transitions associated with the evolution of social parasitism in this genus are largely unexplored. To test competing hypotheses regarding the origins and evolution of social parasitism, we reconstructed a global phylogeny of Formica ants. The genus originated in the Old World ∼30 Ma ago and dispersed multiple times to the New World and back. Within Formica , obligate dependent colony-founding behavior arose once from a facultatively polygynous common ancestor practicing independent and facultative dependent colony foundation. Temporary social parasitism likely preceded or arose concurrently with obligate dependent colony founding, and dulotic social parasitism evolved once within the obligate dependent colony-founding clade. Permanent social parasitism evolved twice from temporary social parasitic ancestors that rarely practiced colony budding, demonstrating that obligate social parasitism can originate from a facultative parasitic background in socially polymorphic organisms. In contrast to permanently socially parasitic ants in other genera, the high parasite diversity in Formica likely originated via allopatric speciation, highlighting the diversity of convergent evolutionary trajectories resulting in nearly identical parasitic life history syndromes.