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

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. Acromyrmex leaf-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 American Acromyrmex species to study how different selective pressures influence the evolution of polygyny and polyandry. We show that Acromyrmex species 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 in Acromyrmex leaf-cutting ants. Significance statement 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.

Synchronized swarming: Harmonic convergence and acoustic mating dynamics in the malaria mosquito Anopheles gambiae

The mosquito Anopheles gambiae is a major African malaria vector, transmitting parasites responsible for significant mortality and disease burden. Malaria declines have stagnated recently due to widespread insecticide resistance among vector populations. Flight acoustics are essential to mosquito mating biology and represent promising alternative targets for mosquito control. However, mosquito swarm acoustics data are limited. Here, for the first time, we present detailed analyses of free-flying male and female An. gambiae flight tones and their harmonization (harmonic convergence) over a complete swarm sequence. Audio analysis of single-sex swarms showed elevated male or female flight tone frequencies and amplitudes during swarming flight with gradual declines to pre-swarm levels over an approximately 35-min period. Analysis of mixed-sex swarms revealed additional increases in flight tone frequencies and amplitudes due to mating activity. Data from mixed-sex swarms suggest harmonic convergence during swarming enhances the efficiency of female detection by synchronizing male and female baseline swarm tones. Further, data from experiments using female swarm tone playbacks to males indicate that harmonic convergence during mating interactions coordinates male scramble competition by acoustically masking mating couple flight tones. These findings advance our knowledge of mosquito swarm acoustics, providing vital information for reproductive control strategies.

Insights into how development and life-history dynamics shape the evolution of venom

Venomous animals are a striking example of the convergent evolution of a complex trait. These animals have independently evolved an apparatus that synthesizes, stores, and secretes a mixture of toxic compounds to the target animal through the infliction of a wound. Among these distantly related animals, some can modulate and compartmentalize functionally distinct venoms related to predation and defense. A process to separate distinct venoms can occur within and across complex life cycles as well as more streamlined ontogenies, depending on their life-history requirements. Moreover, the morphological and cellular complexity of the venom apparatus likely facilitates the functional diversity of venom deployed within a given life stage. Intersexual variation of venoms has also evolved further contributing to the massive diversity of toxic compounds characterized in these animals. These changes in the biochemical phenotype of venom can directly affect the fitness of these animals, having important implications in their diet, behavior, and mating biology. In this review, we explore the current literature that is unraveling the temporal dynamics of the venom system that are required by these animals to meet their ecological functions. These recent findings have important consequences in understanding the evolution and development of a convergent complex trait and its organismal and ecological implications.

Mating-regulated atrial proteases control reinsemination rates in Anopheles gambiae females

Anopheles gambiae mosquitoes are the most important vectors of human malaria. The reproductive success of these mosquitoes relies on a single copulation event after which the majority of females become permanently refractory to further mating. This refractory behavior is at least partially mediated by the male-synthetized steroid hormone 20-hydroxyecdysone (20E), which is packaged together with other seminal secretions into a gelatinous mating plug and transferred to the female atrium during mating. In this study, we show that two 20E-regulated chymotrypsin-like serine proteases specifically expressed in the reproductive tract of An. gambiae females play an important role in modulating the female susceptibility to mating. Silencing these proteases by RNA interference impairs correct plug processing and slows down the release of the steroid hormone 20E from the mating plug. In turn, depleting one of these proteases, the Mating Regulated Atrial Protease 1 (MatRAP1), reduces female refractoriness to further copulation, so that a significant proportion of females mate again. Microscopy analysis reveals that MatRAP1 is localized on a previously undetected peritrophic matrix-like structure surrounding the mating plug. These data provide novel insight into the molecular mechanisms shaping the post-mating biology of these important malaria vectors.

Inclusive Fitness of Male and Facultatively Social Female Nesting Behavior in the Socially Polymorphic Bee, Ceratina australensis (Hymenoptera: Xylocopinae)

Male hymenopterans do not typically provide help with nest construction or maintenance. This is thought to be due to the decreased relatedness of males to their siblings compared to sisters, and selection for outbreeding resulting in male dispersal from natal nesting sites. However, some instances of male ‘helping’ behaviors have been observed and can usually be explained by increased access to mating with resident females. Here we report on the first observations of cohabiting males within the nests of reproductive females of the facultatively social small carpenter bee, Ceratina australensis. Social nesting in C. australensis occurs at a consistently low rate across populations. We used microsatellites markers to determine relatedness, combined with 3 yr of nest demographic data collected across three populations, to assess the relative fitness of reproductive, nonreproductive, and male individuals cohabiting in reproductive nests. We found that males were brothers of reproductive females, both remaining in their natal nest. However, there was no evidence that they were mating with their sisters across all nests observed. Males in reproductive nests did not gain any direct or indirect fitness benefits as they did not sire any brood and their presence did not increase brood productivity or survivorship. It is possible that males were waiting to mate with nieces who had not yet emerged. Why males were tolerated remains unknown. Mating biology is an important consideration in social theory which requires additional empirical studies. Future long-term studies are needed to capture unusual social behaviors including male nesting behaviors.

Not the Honey Bee (Apis mellifera L.) Queen, but the Drone Determines the Termination of the Nuptial Flight and the Onset of Oviposition - The Polemics, Abnegations, Corrections and Supplements

This paper emphasizes the topics concerning honey bee (Apis mellifera L.) mating biology, which have not been described in the recently published book of Koeniger et al. (2014). At the beginning of natural mating, the drone becomes paralyzed. However, the muscles in the abdomen continuously contract shrinking the abdomen till mating has ended and the pair have separated. It is not the queen that ends the nuptial flight. The termination of the nuptial flight is determined by the drone, which fails to remove the mating sign of the previous drone from the sting chamber of the queen. The mating sign originates from two or more drones. The queen also does not determine the age at which she starts oviposition. It is the last drone, which tried to mate, but failed to remove the mating sign of the predecessor, that determines the age that the queen starts oviposition. The book of Koeniger et al. (2014), together with this paper, present the current knowledge of the mating biology of honey bees.

Extreme cost of rivalry in a monandrous species: male–male interactions result in failure to acquire mates and reduced longevity

Mating system variation is profound in animals. In insects, female willingness to remate varies from mating with hundreds of males (extreme polyandry) to never remating (monandry). This variation in female behaviour is predicted to affect the pattern of selection on males, with intense pre-copulatory sexual selection under monandry compared to a mix of pre- and post-copulatory forces affecting fitness under polyandry. We tested the hypothesis that differences in female mating biology would be reflected in different costs of pre-copulatory competition between males. We observed that exposure to rival males early in life was highly costly for males of a monandrous species, but had lower costs in the polyandrous species. Males from the monandrous species housed with competitors showed reduced ability to obtain a mate and decreased longevity. These effects were specific to exposure to rivals compared with other types of social interactions (heterospecific male and mated female) and were either absent or weaker in males of the polyandrous species. We conclude that males in monandrous species suffer severe physiological costs from interactions with rivals and note the significance of male–male interactions as a source of stress in laboratory culture.