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1. Multi-queen breeding is associated with the origin of inquiline social parasitism in ants

   https://doi.org/10.1038/s41598-022-17595-0  

   Dahan, Romain A. ; Rabeling, Christian ( August 2022 , Scientific Reports)

   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, wemore »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.

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2. Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

   https://doi.org/10.1007/s00265-021-03113-1  

   Dahan, Romain A. ; Grove, Nathan K. ; Bollazzi, Martin ; Gerstner, Benjamin P. ; Rabeling, Christian ( December 2021 , Behavioral Ecology and Sociobiology)

   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 significantmore »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.

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3. Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa

   https://doi.org/10.1002/ece3.10046  

   Espeland, Marianne ; Chazot, Nicolas ; Condamine, Fabien L. ; Lemmon, Alan R. ; Lemmon, Emily Moriarty ; Pringle, Ernest ; Heath, Alan ; Collins, Steve ; Tiren, Wilson ; Mutiso, Martha ; et al ( May 2023 , Ecology and Evolution)

   Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto‐predaceousLepidochrysopsbutterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time‐calibrated phylogeny forLepidochrysopsand its closest, non‐parasitic relatives in theEuchrysopssection (Poloyommatini). We estimated ancestral areas across the phylogeny with process‐based biogeographical models and diversification rates relying on time‐variable and clade‐heterogeneous birth‐death models. TheEuchrysopssection originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non‐parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto‐predaceousLepidochrysopslineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of theEuchrysopssection, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto‐predaceous life history in species ofLepidochrysops, with ant nests likely providing caterpillars amore »safe refuge from fire and a source of food when vegetation was scarce.

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4. Relaxed selection underlies genome erosion in socially parasitic ant species

   https://doi.org/10.1038/s41467-021-23178-w  

   Schrader, Lukas ; Pan, Hailin ; Bollazzi, Martin ; Schiøtt, Morten ; Larabee, Fredrick J. ; Bi, Xupeng ; Deng, Yuan ; Zhang, Guojie ; Boomsma, Jacobus J. ; Rabeling, Christian ( December 2021 , Nature Communications)

   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.
5. An organizing feature of bumble bee life history: worker emergence promotes queen reproduction and survival in young nests.

   https://doi.org/https://doi.org/10.1093/conphys/coab047  

   Sarro E, Sun P ( January 2021 , Conservation physiology)

   Bumble bee queens initiate nests solitarily and transition to living socially once they successfully rear their first cohort of offspring. Bumble bees are disproportionately important for early season pollination, and many populations are experiencing dramatic declines. In this system, the onset of the social stage is critical for nest survival, yet the mechanisms that facilitate this transition remain understudied. Further, the majority of conservation efforts target the social stage of the bumble bee life cycle and do not address the solitary founding stage. We experimentally manipulated the timing of worker emergence in young nests of bumble bee (Bombus impatiens) queens to determine whether and how queen fecundity and survival are impacted by the emergence of workers in the nest. We found that queens with workers added to the nest exhibit increased ovary activation, accelerated egg laying, elevated juvenile hormone (JH) titres and also lower mortality relative to solitary queens. We also show that JH is more strongly impacted by the social environment than associated with queen reproductive state, suggesting that this key regulator of insect reproduction has expanded its function in bumble bees to also influence social organization. We further demonstrate that these effects are independent of queen social history,more »suggesting that this underlying mechanism promoting queen fecundity is reversible and short lived. Synchronization between queen reproductive status and emergence of workers in the nest may ultimately increase the likelihood of early nesting success in social systems with solitary nest founding. Given that bumble bee workers regulate queen physiology as we have demonstrated, the timing of early worker emergence in the nest likely impacts queen fitness, colony developmental trajectories and ultimately nesting success. Collectively, our findings underline the importance of conservation interventions for bumble bees that support the early nesting period and facilitate the production and maintenance of workers in young nests« less