Sexual cooperation: mating increases longevity in ant queens

Divergent reproductive interests of males and females often cause sexual conflict . Males of many species manipulate females by transferring seminal fluids that boost female short-term fecundity while decreasing their life expectancy and future reproductivity . The life history of ants, however, is expected to reduce sexual conflict; whereas most insect females show repeated phases of mating and reproduction, ant queens mate only during a short period early in life and undergo a lifelong commitment to their mates by storing sperm . Furthermore, sexual offspring can only be reared after a sterile worker force has been built up . Therefore, the males should also profit from a long female lifespan. In the ant Cardiocondyla obscurior, mating indeed has a positive effect on the lifetime reproductive success of queens. Queens that mated to either one fertile or one sterilized male lived considerably longer and started laying eggs earlier than virgin queens. Only queens that received viable sperm from fertile males showed increased fecundity. The lack of a trade-off between fecundity and longevity is unexpected, given evolutionary theories of aging . Our data instead reveal the existence of sexual cooperation in ants.     

Cuticular lipid profiles of fertile and non-fertile Cardiocondyla ant queens

Both mating and reproduction strongly affect the physiology of insect females. In the ant Cardiocondyla obscurior, a comparison among virgin queens, mated queens, and queens mated with sterilized males ("sham-mated") allows to separate the different effects of mating and egg laying. Here, we investigate whether and how different mating status is reflected in the cuticular lipid profiles of queens, i.e., the blend of chemicals that is thought to signal a queen's fertility. Surprisingly, discriminant analyses failed to reliably distinguish among virgin, mated, and sham-mated queens. A generalized linear model on individual substances showed only very subtle differences. While mating appeared to be positively associated with the proportions of 3-MeC(25,) 11-/13-MeC(27), 5-MeC(27), 3-MeC(27), and 12-/14-MeC(28) and negatively with C(27:1), fecundity was negatively associated with C(29:1), C(31:1), and a sterol derivative. We discuss these results in the light of the special life history of C. obscurior, with completely sterile workers and low egg laying rates in queens.     

Queen number influences the timing of the sexual production in colonies of Cardiocondyla ants

Wingless males of the ant genus Cardiocondyla engage in fatal fighting for access to female sexual nestmates. Older, heavily sclerotized males are usually capable of eliminating all younger rivals, whose cuticle is still soft. In Cardiocondyla sp. A, this type of local mate competition (LMC) has turned the standard pattern of brood production of social insects upside down, in that mother queens in multi-queen colonies produce extremely long-lived sons very early in the life cycle of the colony. Here, we investigated the emergence pattern of sexuals in two species with LMC, in which males are much less long-lived. Queens of Cardiocondyla obscurior and Cardiocondyla minutior reared their first sons significantly earlier in multi-queen than in single-queen societies. In addition, first female sexuals also emerged earlier in multi-queen colonies, so that early males had mating opportunities. Hence, the timing of sexual production appears to be well predicted by evolutionary theory, in particular by local mate and queen-queen competition.     

Mating with stressed males increases the fitness of ant queens

Background

According to sexual conflict theory, males can increase their own fitness by transferring substances during copulation that increase the short-term fecundity of their mating partners at the cost of the future life expectancy and re-mating capability of the latter. In contrast, sexual cooperation is expected in social insects. Mating indeed positively affects life span and fecundity of young queens of the male-polymorphic ant Cardiocondyla obscurior, even though males neither provide nuptial gifts nor any other care but leave their mates immediately after copulation and die shortly thereafter.

Principal Findings

Here, we show that mating with winged disperser males has a significantly stronger impact on life span and reproductive success of young queens of C. obscurior than mating with wingless fighter males.

Conclusions

Winged males are reared mostly under stressful environmental conditions, which force young queens to disperse and found their own societies independently. In contrast, queens that mate with wingless males under favourable conditions usually start reproducing in the safety of the established maternal nest. Our study suggests that males of C. obscurior have evolved mechanisms to posthumously assist young queens during colony founding under adverse ecological conditions.     

Lifetime reproductive success and longevity of queens in an annual social insect

Although central to understanding life‐history evolution, the relationship between lifetime reproductive success and longevity remains uncertain in many organisms. In social insects, no studies have reported estimates of queens’ lifetime reproductive success and longevity within populations, despite the importance of understanding how sociality and associated within‐group conflict affect life‐history traits. To address this issue, we studied two samples of colonies of the annual bumblebee, Bombus terrestris audax, reared from wild‐caught queens from a single population. In both samples, queens’ lifetime reproductive success, measured as either queens’ inclusive fitness or as total biomass of queen‐produced sexuals (new queens and males), was significantly positively associated with queen longevity, measured from the day the first worker was produced. We suggest that a positive relationship between reproductive success and longevity was inherited from nonsocial ancestors showing parental care and maintained, at least in part, because the presence of workers buffers queens against extrinsic mortality.     

Back to one: consequences of derived monogyny in an ant with polygynous ancestors

The number of queens per colony is of fundamental importance in the life history of social insects. Multiple queening (polygyny), with dependent colony founding by budding, has repeatedly evolved from ancestral single queening (monogyny) and independent founding by solitary queens in waSPS, bees and ants. By contrast, the reversal to monogyny appears to be rare, as polygynous queens often lack morphological adaptations necessary for dispersal and independent colony founding. In the ant genus Cardiocondyla, monogynous species evolved from polygynous ancestors. Here, we show that queens of monogynous species found their colonies independently, albeit in an unusual way: they mate in the maternal nest, disperse on foot and forage during the founding phase. This reversal appears to be associated with the occurrence of a wing polymorphism, which reflects a trade-off between reproduction and dispersal. Moreover, queens of monogynous species live considerably longer than queens in related polygynous taxa, suggesting that queen life span is a plastic trait.     

Intrinsic survival advantage of social insect queens depends on reproductive activation

The central trade‐off between reproduction and longevity dominates most species' life history. However, no mortality cost of reproduction is apparent in eusocial species, particularly social insects in the order Hymenoptera: one or a few individuals (typically referred to as queens) in a group specialize on reproduction and are generally longer lived than all other group members (typically referred to as workers), despite having the same genome. However, it is unclear whether this survival advantage is due to social facilitation by the group or an intrinsic, individual property. Furthermore, it is unknown whether the correlation between reproduction and longevity is due to a direct mechanistic link or an indirect consequence of the social role of the reproductives. To begin addressing these questions, we performed a comparison of queen and worker longevity in the ant Cardiocondyla obscurior under social isolation conditions. Survival of single queens and workers was compared under laboratory conditions, monitoring and controlling for brood production. Our results indicate that there is no intrinsic survival advantage of queens relative to workers unless individuals are becoming reproductively active. This interactive effect of caste and reproduction on life expectancy outside of the normal social context suggests that the positive correlation between reproduction and longevity in social insect queens is due to a direct link that can activate intrinsic survival mechanisms to ensure queen longevity.     

Adaptive production of fighter males: queens of the ant Cardiocondyla adjust the sex ratio under local mate competition

Hamilton's concept of local mate competition (LMC) is the standard model to explain female-biased sex ratios in solitary Hymenoptera. In social Hymenoptera, however, LMC has remained controversial, mainly because manipulation of sex allocation by workers in response to relatedness asymmetries is an additional powerful mechanism of female bias. Furthermore, the predominant mating systems in the social insects are thought to make LMC unlikely. Nevertheless, several species exist in which dispersal of males is limited and mating occurs in the nest. Some of these species, such as the ant Cardiocondyla obscurior, have evolved dimorphic males, with one morph being specialized for dispersal and the other for fighting with nest-mate males over access to females. Such life history, combining sociality and alternative reproductive tactics in males, provides a unique opportunity to test the power of LMC as a selective force leading to female-biased sex ratios in social Hymenoptera. We show that, in concordance with LMC predictions, an experimental increase in queen number leads to a shift in sex allocation in favour of non-dispersing males, but does not influence the proportion of disperser males. Furthermore, we can assign this change in sex allocation at the colony level to the queens and rule out worker manipulation.     

Mating opportunity and the evolution of sex-specific mortality rates in a butterfly

Life history theory predicts that organisms should only invest resources into intrinsic components of life span to the degree that it pays off in terms of reproductive success. Here, we investigate if the temporal distribution of mating opportunities may have influenced the evolution of intrinsic mortality rates in the butterfly Pararge aegeria (Satyrinae). In this species, females mate only once and the frequency of male mating opportunities depends on the temporal emergence pattern of virgin females. As expected, in a population from Madeira where females emerge continuously throughout the year, there was no sex difference in adult life span, while in a Swedish population with synchronised female emergence, males had significantly shorter life spans compared to females. A logistic mortality model provided the best fit to the observed change in age-specific mortality and all categories reached an asymptotic mortality rate of a similar magnitude. However, the Swedish males reached this mortality plateau more rapidly than the other categories. External mortality, due to water and food limitation, affected the pattern of sex-specific mortality but males from Sweden still had higher rates of mortality compared to all other categories. We argue that selection on male longevity is likely to be weaker in Sweden because under synchronised emergence, all females emerge and mate within a short period of time, after which male reproductive value will quickly approach zero. On Madeira, however, male reproductive value decrease more slowly with age since the probability of finding a receptive female is constant over the year. Received: 29 July 1999 / Accepted: 23 August 1999     

Proximate Determinants of Reproductive Skew in Polygyne Colonies of the Ant Formica fusca

Understanding the determinants of reproductive skew (the partitioning of reproduction among co‐breeding individuals) is one of the major questions in social evolution. In ants, multiple‐queen nests are common and reproductive skew among queens has been shown to vary tremendously both within and between species. Proximate determinants of skew may be related to both queen and worker behaviour. Queens may attempt to change their reproductive share through dominance interactions, egg eating and by changing individual fecundity. Conversely, workers are in a position to regulate the reproductive output of queens when rearing the brood. This paper investigates queen behaviour at the onset of egg laying and the effect of queen fecundity and worker behaviour on brood development and reproductive shares of multiple queens in the ant Formica fusca. The study was conducted in two‐queen laboratory colonies where the queens produced only worker offspring. The results show that in this species reproductive apportionment among queens is not based on dominance behaviour and aggression, but rather on differences in queen fecundity. We also show that, although the queen fecundity at the onset of brood rearing is a good indicator of her final reproductive output, changes in brood composition occur during brood development. Our results highlight the importance of queen fecundity as a major determinant of her reproductive success. They furthermore suggest that in highly derived polygyne species, such as the Formica ants, direct interactions as a means for gaining reproductive dominance have lost their importance.     

Genome-wide analysis reveals differences in brain gene expression patterns associated with caste and reproductive status in honey bees (Apis mellifera)

A key characteristic of eusocial species is reproductive division of labour. Honey bee colonies typically have a single reproductive queen and thousands of sterile workers. Adult queens differ dramatically from workers in anatomy, physiology, behaviour and lifespan. Young female workers can activate their ovaries and initiate egg laying; these 'reproductive' workers differ from sterile workers in anatomy, physiology, and behaviour. These differences, however, are on a much smaller scale than those observed between the queen and worker castes. Here, we use microarrays to monitor expression patterns of several thousand genes in the brains of same-aged virgin queens, sterile workers, and reproductive workers. We found large differences in expression between queens and both worker groups (~2000 genes), and much smaller differences between sterile and reproductive workers (221 genes). The expression patterns of these 221 genes in reproductive workers are more queen-like, and may represent a core group of genes associated with reproductive physiology. Furthermore, queens and reproductive workers preferentially up-regulate genes associated with the nurse bee behavioural state, which supports the hypothesis of an evolutionary link between worker division of labour and molecular pathways related to reproduction. Finally, several functional groups of genes associated with longevity in other species are significantly up-regulated in queens. Identifying the genes that underlie the differences between queens, sterile workers, and reproductive workers will allow us to begin to characterize the molecular mechanisms underlying the evolution of social behaviour and large-scale remodelling of gene networks associated with polyphenisms.     

Queen fecundity and reproductive skew in the termite Nasutitermes corniger

A major goal of studies on social animals is to understand variation in reproduction within and between groups. We used hierarchical regressions to analyze oviposition rates in the neotropical termite Nasutitermes corniger, a species with both monogynous and polygynous colonies. Queen fecundity was a non-linear, saturating function of queen weight. Greater queen weight was associated with larger nest size and with lower numbers of queens per nest, suggesting competition among queens for resources acquired by the colony. The collective egglaying rate of pairs of queens exceeded that of single queens, but further increases in queen number did not raise total fecundity. Skew in oviposition rates, as quantified by Morisita’s index I _δ, averaged 1.2, indicating inequalities in reproductive rates that are only moderately greater than expected for random apportionment. The leveling off of oviposition with increasing queen weight suggests that it is costly for individual females to produce eggs at high rates, which could favor tolerance of reproduction by other females, reducing reproductive skew. We hypothesize that the incentive to tolerate reproduction by other females is especially pronounced for heavier queens, because these queens are close to the limit of their own reproductive capacity. Consistent with this hypothesis, skew in oviposition rates was inversely related to the mean weight of queens within a nest. Received 8 March 2007; revised 17 September 2007; accepted 3 October 2007.     

Queen reproductive state modulates pheromone production and queen-worker interactions in honeybees

The mandibular glands of queen honeybees produce a pheromone that modulates many aspects of worker honeybee physiology and behavior and is critical for colony social organization. The exact chemical blend produced by the queen differs between virgin and mated, laying queens. Here, we investigate the role of mating and reproductive state on queen pheromone production and worker responses. Virgin queens, naturally mated queens, and queens instrumentally inseminated with either semen or saline were collected 2 days after mating or insemination. Naturally mated queens had the most activated ovaries and the most distinct chemical profile in their mandibular glands. Instrumentally inseminated queens were intermediate between virgins and naturally mated queens for both ovary activation and chemical profiles. There were no significant differences between semen- and saline-inseminated queens. Workers were preferentially attracted to the mandibular gland extracts from queens with significantly more activated ovaries. These studies suggest that the queen pheromone blend is modulated by the reproductive status of the queens, and workers can detect these subtle differences and are more responsive to queens with higher reproductive potential. Furthermore, it appears as if insemination substance does not strongly affect physiological characteristics of honeybee queens 2 days after insemination, suggesting that the insemination process or volume is responsible for stimulating these early postmating changes in honeybee queens.     

Age-specific patterns of reproduction in White-tailed and Willow Ptarmigan Lagopus leucurus and L. lagopus

Although many studies report a difference in reproductive success between old and young birds, little is known about how, why and when productivity changes as individuals age. We examined age-dependent reproduction in two bird species that inhabit harsh tundra environments: White-tailed Ptarmigan Lagopus leucurus in alpine areas and Willow Ptarmigan Lagopus lagopus in subarctic Canada. We evaluated reproductive performance in the light of three hypotheses: constraint, restraint and selection. Using cross-sectional and longitudinal data, we observed significant age effects in seven of the eight life history and behavioural traits examined for the two species. However, the pattern of age effects variedconsiderably across life history stages; younger birds generally had smaller clutches, later laying dates and poorer spring body condition, but the nesting success did not vary with age. Brood-rearing and renesting abilities were greater for older parents. The oldest age class of White-tailed Ptarmigan showed reproductive senescence for laying date and clutch size but fledged such a large proportion of the brood that they had the highest overall production of any class. It thus appears that parental experience can compensate for reduced physical ability to produce eggs. Annual mortality rates for breeding females were U-shaped for White-tailed Ptarmigan, with higher rates for young and old birds, but mortality did not change with age in Willow Ptarmigan. Overall, the two species differed in the presence of age dependence for only two traits (renesting ability and annual survival). Age-dependent effects were generally greater for White-tailed Ptarmigan than for Willow Ptarmigan. The patterns of mortality and fecundity we observed in ptarmigan provide general support for the constraint hypothesis of reproductive performance. By examining discrete stages of reproduction, we identified the life history stages where age effects occur and propose proximate mechanisms responsible for these effects.     

Patterns of age-specific means and genetic variances of mortality rates predicted by the mutation-accumulation theory of ageing

A general quantitative genetic model of mutations with age-specific deleterious effects is developed. It is shown that, for the simplest case of a species with age-independent reproductive rates and extrinsic adult mortality rates, and no pleiotropic effects of age-specific mutations, exponential increases with age of both the mean and additive genetic variance of age-specific mortality rates are expected. Models where age-specific mutations have pleiotropic effects on mortality that extend either throughout adult life, or are confined to juvenile stages, produce equilibria with exponential increases in the mean and additive variance of mortality rates during much of adult life. However, the rates of increase diminish late in life, and can even become zero. Predictions concerning the additive genetic correlations in mortality rates between different ages are also developed. The predictions of the models are compared with data on humans and Drosophila.     

Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites

Abstract.

• 1 In natural populations, colonies of bumble bees vary in many important life history traits, such as colony size and age at maturity, or the number and sex of reproductives produced. We investigated how the presence of parasites in field populations of the bumble bee Bombus lucorum L. relates to variation in life history traits and reproductive performance. A total of thirty-six colonies was placed in accessible nest sites in the field and monitored at regular intervals throughout a season.
• 2 Among the life history correlates, early nest foundation was strongly associated with large maximum colony size, old age and large size at maturity, and this in turn with successful production of males and queens, as well as with the number of sexuals produced. Overall, reproductive success was highly skewed with only five colonies producing all the queens. Sixteen colonies failed to reproduce altogether.
• 3 The social parasite Psithyrus was abundant early in the Bombus colony cycle and preferentially invaded host nests with many first brood workers and thus disproportionately large size, i.e. those colonies that would otherwise be more likely to reproduce or produce (daughter) queens rather than males. To prevent nest loss, Psithyrus had to be removed soon after invasion. Therefore, the effects reported here can only be crude estimates.
• 4 Parasitoid conopid flies are likely to cause heavy worker mortality when sexuals are reared by the colonies. Their inferred effect was a reduction in biomass that could be invested in sexuals as well as a shift in the sex ratio at the population level resulting from failure to produce queens. We suggest to group the inferred correlates into ‘early events’ surrounding colony initiation and social parasitism, and ‘late events’ surrounding attained colony size in summer and parasitism by conopid flies. Our evidence thus provides a heuristic approach to understand the factors that affect reproductive success of Bombus colonies.

     

Reproductive parameters vary with social and ecological factors in the polygynous ant Formica exsecta

Due to their haplo‐diploid sex determination system and the resulting conflict over optimal sex allocation between queens and workers, social Hymenoptera have become important model species to study variation in sex allocation. While many studies indeed reported sex allocation to be affected by social factors such as colony kin structure or queen number, others, however, found that sex allocation was impacted by ecological factors such as food availability. In this paper, we present one of the rare studies that simultaneously investigated the effects of social and ecological factors on social insect nest reproductive parameters (sex and reproductive allocation, nest productivity) across several years. We found that the sex ratio was extremely male biased in a polygynous (multiple queens per nest) population of the ant Formica exsecta. Nest‐level sex allocation followed the pattern predicted by the queen‐replenishment hypothesis, which holds that gynes (new queens) should only be produced and recruited in nests with low queen number (i.e. reduced local resource competition) to ensure nest survival. Accordingly, queen number (social factor) was the main determinant on whether a nest produced gynes or males. However, ecological factors had a large impact on nest productivity and therefore on a nest's resource pool, which determines the degree of local resource competition among co‐breeding queens and at what threshold in queen number nests should switch from male to gyne production. Additionally, our genetic data revealed that gynes are recruited back to their parental nests after mating. However, our genetic data are also consistent with some adult queens dispersing on foot from nests where they were produced to nests that never produced queens. As worker production is reduced in gyne‐producing nests, queen migration might be offset by workers moving in the other direction, leading to a nest network characterized by reproductive division of labour. Altogether our study shows that both, social and ecological factors can influence long‐term nest reproductive strategies in insect societies.     

Demographic analyses of organophosphate-resistant and susceptible strains of greenhouse whitefly, Trialeurodes vaporariorum, on three cotton cultivars

Laboratory experiments were conducted using organophosphate-resistant and susceptible strains of greenhouse whitefly, Trialeurodes vaporariorum Westwood, to assess age-specific vital rates in individually-held adults, and development and survival in preadults on three cotton cultivars at 27±1 °C, 50±10% RH, and a photoperiod of 16:8 (L:D). Female whiteflies lived longer than males, with a maximum life expectancy of 29 days. Heaviest egg laying occurred at ages between 7 and 18 days when individual whiteflies laid > 10 eggs/day. Greenhouse whitefly populations doubled weekly, with stable age distribution of 63% eggs, 28% larvae, 5% pupae, and 4% adults. Analysis of various life history parameters that combine aspects of survival, developmental rates, and fecundity indicated no consistent differences in reproductive fitness between the two greenhouse whitefly strains. Of the three cotton cultivars tested, Pima S-6 was most susceptible, Acala SJ-2 was intermediate and Gumbo 500 was most resistant to greenhouse whitefly. Resistance of Gumbo 500 was expressed as slower developmental rates, reduced survival to adulthood, lower reproductive rates, and lower intrinsic rate of increase.