Courtship with two spoons—Anatomy and presumed function of the bizarre antennae of Cardiocondyla zoserka ant males

Mating in ants often occurs on the wing during nuptial flights or on the ground when scattered female sexuals attract males by pheromones. In both scenarios, there is little opportunity for males to engage in prolonged aggressive competition or elaborate courtship displays. Male morphology is therefore adapted to locating female sexuals and mating, and it lacks specific weapons or other traits associated with courtship. In contrast, sexuals of the ant genus Cardiocondyla typically mate in their natal nests. As a consequence, in many species winged males have been replaced by wingless fighter or territorial males, which kill or expel rival males with their strong mandibles and show complex mating behavior. However, no wingless males are known from Cardiocondyla zoserka from West Africa, and instead, winged males have evolved a bizarre secondary sexual trait: uniquely shaped antennae with spoon‐like tips that show heavily sculptured ventral surfaces with numerous invaginations. We here report on the courtship behavior of C. zoserka males and describe antennal glands with class 3 gland cells, which presumably secrete a close range sex pheromone. Antennal glands have not yet been found in males of other ant species, including a close relative of C. zoserka, suggesting that in ants with intranidal mating sexual selection can rapidly lead to highly divergent adaptations and the evolution of novel structures.     

Decision-making conditions for intra- or inter-nest mating of winged males in the male-dimorphic ant <Emphasis Type="Italic">Cardiocondyla minutior</Emphasis>

Only winged male and female ants generally mate through nuptial flight during the reproductive season. In the ants of Cardiocondyla, the males show wing dimorphism and their reproductive strategies differ depending on the differences in wing morphology. It has been suggested that wingless “ergatoid” males bearing very similar external morphologies to workers mate within natal nests, whereas winged males bearing typical ant male morphology disperse from their nests to mate. However, some behavioral observations suggest that the winged males of some Cardiocondyla ants such as C. obscurior and C. minutior may mate within natal nests before dispersion. We evaluated the factors affecting the mating behaviors of the winged males of C. minutior under laboratory conditions. We found that (1) the winged males remained and mated with virgin females in natal nests when either virgin winged females or the relatively mature pupae of winged females (i.e., at least 10 days) were present in the nest, (2) the winged males dispersed to adjacent nests with virgin winged females when only mated queens and the relatively young pupae of winged females (i.e., <9 days) were present in the nest, and (3) all winged males were accepted by the workers of non-natal nests irrespective of the distance from the natal nests in the field. Although most ergatoid males were accepted by the workers of close non-natal nests, they were all attacked and killed by the workers of distant non-natal nests. These results suggest that intra-nest mating and the dispersion of the winged males of C. minutior are facultatively determined by the condition of winged females (virginity and relative pupal age) in natal nests. Furthermore, our results suggest that winged males are likely to seek mating partners chemically and to mate with virgin winged females.     

Genetic structure and reproductive strategy of the ant Cardiocondyla elegans: strictly monogynous nests invaded by unrelated sexuals

Cardiocondyla elegans is a Mediterranean ant that nests on river banks. It rears only wingless (ergatoid) males that live peacefully in the same nest as opposed to other species of the same genus, which have both peaceful, winged and mutually aggressive 'ergatoid' males. Using microsatellite analysis, we investigated the genetic structure of 21 colonies from three different locations as well as the parentage of sexuals of two colonies of C. elegans. We show that C. elegans is strictly monogynous, and that its nests can contain foreign sexuals. The presence of alien sexuals inside ant nests is described for the first time and probably counteracts inbreeding resulting from matings between siblings. In the laboratory, aggression tests showed that workers only allow alien males to enter their nests, while all winged female sexuals attempting to enter were attacked. Nevertheless, the presence of alien female sexuals in nests in the field seems to result from active carrying behaviour by workers during the reproductive period.     

Mate guarding and alternative reproductive tactics in the ant Hypoponera opacior

In many animals, males have evolved weapons, elaborate courtship displays, or costly ornaments to increase their reproductive success. Ants, in contrast, commonly mate during nuptial flights, in which males do not profit from fighting or attempting to monopolize females. However, where mating occurs in the nest, males can use other reproductive tactics. We found that wingless (apterous) males of Hypoponera opacior sat on top of queen cocoons, inserted their genitalia into the cocoons and remained in copula with cocooned queens for up to 40 h. These males were tolerant of each other; fighting was never recorded. Our observations therefore suggest that wingless males of H. opacior ensure reproduction by copulatory mate guarding. This strategy, although time consuming, presumably reduces the likelihood of subsequent inseminations by other males. Apterous H. opacior males have only a limited amount of sperm available: histological preparations showed that, in contrast to Cardiocondyla fighter males, the testes degenerate in early adult life. Males ofH. opacior have relatively few mating opportunities. Although some wingless males were reproductively active for more than 3 weeks, we observed a maximum of only six matings per male, with a mean slightly above one. SomeH. opacior males used an alternative reproductive tactic of dispersal and outbreeding. We found colonies headed by single, dealate queens, which did not rear wingless sexuals but presumably reproduced through winged reproductives that mate in nuptial flights. The social structure of those colonies contrasted with nests containing wingless reproductives, which were highly polygynous and polydomous.     

Similar Performance of Diploid and Haploid Males in an Ant Species without Inbreeding Avoidance

Under haplodiploidy, a characteristic trait of all Hymenoptera, females develop from fertilised eggs, and males from unfertilised ones. Males are therefore typically haploid. Yet, inbreeding can lead to the production of diploid males that often fail in development, are sterile or are of lower fertility. In most Hymenoptera, inbreeding is avoided by dispersal flights of one or both sexes, leading to low diploid male loads. We investigated causes for the production of diploid males and their performance in a highly inbred social Hymenopteran species. In the ant Hypoponera opacior, inbreeding occurs between wingless sexuals, which mate within the mother nest, whereas winged sexuals outbreed during mating flights earlier in the season. Wingless males mate with queen pupae and guard their mating partners. We found that they mated randomly with respect to relatedness, indicating that males do not avoid mating with close kin. These frequent sib‐matings lead to the production of diploid males, which are able to sire sterile triploid offspring. We compared mating activity and lifespan of haploid and diploid wingless males. As sexual selection acts on the time of emergence and body size in this species, we also investigated these traits. Diploid males resembled haploid ones in all investigated traits. Hence, albeit diploid males cannot produce fertile offspring, they keep up with haploid males in their lifetime mating success. Moreover, by fathering viable triploid workers, they contribute to the colonies' work force. In conclusion, the lack of inbreeding avoidance led to frequent sib‐matings of wingless sexuals, which in turn resulted in the regular production of diploid males. However, in contrast to many other Hymenopteran species, diploid males exhibit normal sexual behaviour and sire viable, albeit sterile daughters.     

Between fighting and tolerance: reproductive biology of wingless males in the ant Cardiocondyla venustula

Male reproductive tactics vary widely across the species of the ant genus Cardiocondyla, from obligatory lethal combat among co‐occurring males to complete mutual tolerance. The African species C. venustula Wheeler, 1908 has an intermediate phylogenetic position between taxa with fighting males and taxa with tolerant males and also shows an intermediate male behavior. Males from 2 native populations in South Africa and a population introduced to Puerto Rico attacked and killed freshly eclosing rivals but rarely engaged in deadly fights with adult competitors. Instead, several males per colony established small “territories” in their natal nests and defended them against other males. Males with a stable territory had more contact with female sexuals than nonterritorial males and more frequently engaged in mating attempts. In controlled choice experiments, female sexuals did not show any preference for particular males. We suggest that male territoriality in C. venustula is an adaptation to the seasonal production of large numbers of female sexuals by multiple mothers.     

THE EVOLUTION OF ALTERNATIVE REPRODUCTIVE TACTICS IN MALE CARDIOCONDYLA ANTS

Alternative reproductive tactics are often associated with discontinuous variation in morphology but may evolve independent from each other. Based on life‐history data and a phylogeny we examine how male morphology and reproductive behavior are linked in the evolution of the ant genus Cardiocondyla. Wingless Cardiocondyla males engage in lethal fighting for access to female sexuals, whereas winged males disperse and mate away from the nest. This basic pattern shows considerable variation across species. A phylogeny based on ～3 kbp sequence data shows that male diphenism and lethal fighting are ancestral traits tightly linked in evolution. Winged males were lost convergently in several species groups, apparently in response to the low probability of encountering female sexuals in nests without a resident fighter male. An early dichotomy separates two clades with alternative male morphologies and fighting behavior, but phenotype and fighting strategy are not correlated with the presence of winged males.     

Alternative mating tactics and extreme male dimorphism in fig wasps

The dimorphisms in morphology and behaviour of male fig wasps are among the most extreme in the animal kingdom, and offer excellent opportunities to test the predictions of certain sexual selection models. Winged males resemble their conspecific females closely, but wingless males are so divergent in form that they have repeatedly been classified into different taxa. Wingless males mate within their natal fig fruits, whereas winged males disperse to mate. Individual species may have winged males, wingless males or both morphs. A key hypothesis proposes that sexual selection on male mating opportunities favours winged males in species with small broods and wingless males in species with large broods. Using data from 114 species in 33 genera, we show that both simple and formal comparative analyses support the correlated evolution of large brood size and male winglessness. Theoretical models further predict that, in male dimorphic species, the proportion of winged males should equal (in cases without local mate competition) or exceed (in cases with local mate competition) the proportion of females developing in fig fruits without wingless males. These predictions are met by eight out of nine male dimorphic species studied. Taken together, the patterns across all species, and between different male dimorphic species, strongly support sexual selection on mating opportunities as the major determinant of male morph ratios in fig wasps.     

Stress grows wings: environmental induction of winged dispersal males in Cardiocondyla ants

Dispersal is advantageous, but, at the same time, it implies high costs and risks. Due to these counteracting selection pressures, many species evolved dispersal polymorphisms, which, in ants, are typically restricted to the female sex (queens). Male polymorphism is presently only known from a few genera, such as Cardiocondyla, in which winged dispersing males coexist with wingless fighter males that mate exclusively inside their maternal nests. We studied the developmental mechanisms underlying these alternative male morphs and found that, first, male dimorphism is not genetically determined, but is induced by environmental conditions (decreasing temperature and density). Second, male morph is not yet fixed at the egg stage, but it differentiates during larval development. This flexible developmental pattern of male morphs allows Cardiocondyla ant colonies to react quickly to changes in their environment. Under good conditions, they invest exclusively in philopatric wingless males. But, when environmental conditions turn bad, colonies start to produce winged dispersal males, even though these males require a many times higher investment by the colony than their much smaller wingless counterparts. Cardiocondyla ants share this potential of optimal resource allocation with other colonial animals and some seed dimorphic plants.     

Assisted dispersal and reproductive success in an ant species with matchmaking

Workers of the ant Cardiocondyla elegans drop female sexuals into the nest entrance of other colonies to promote outbreeding with unrelated, wingless males. Corroborating the results from previous years, we document that carrier and carried female sexuals are typically related and that the transfer initially occurs mostly from their joint natal colonies to unrelated colonies. Female sexuals mate multiply with up to seven genetically distinguishable males. Contrary to our expectation, the colony growth rate of multiple‐mated and outbred female sexuals was lower than that of inbred or single‐mated females, leading to the question of why female sexuals mate multiply at all. Despite the obvious costs, multiple mating might be a way for female sexuals to “pay rent” for hibernation in an alien nest. We argue that in addition to evade inbreeding depression from regular sibling mating over many generations, assisted dispersal might also be a strategy for minimizing the risk of losing all reproductive investment when nests are flooded in winter.     

Effects of Social Structure on the Behaviour and Performance of Alternative Reproductive Phenotypes in Male Rock Shrimp, Rhynchocinetes typus

Males that adopt alternative mating tactics within a conditional strategy often undergo costly morphological changes when switching to the next phenotype during ontogeny. Whether costs of changing to a subsequent reproductive phenotype are outweighed by a higher mating probability may depend on the frequencies of different phenotypes in a group of competitors. Benefits and costs associated with different phenotype frequencies depend on interactions within and between alternative phenotypes, but the underlying behavioural mechanisms have rarely been studied. Herein, we used the rock shrimp Rhynchocinetes typus as a model: ontogenetic male stages of this species differ in morphological and behavioural traits that indicate alternative reproductive phenotypes. The small, subordinate, male stage (typus) develops via several intermediate stages (intermedius) to the dominant male stage (robustus): in competitive interactions the typus males usually employ the sneaking tactic, while the robustus males invariably employ the monopolizing fighter tactic. In laboratory experiments, we manipulated phenotype frequencies to examine whether there are frequency‐dependent effects on searching behaviour, aggressiveness and mating probability. With increasing frequency of robustus males, the rate of aggressive interactions among them increased. Furthermore, robustus males increased walking velocity when more than one robustus male was present. In contrast, typus males did not adjust their searching or aggressive behaviour. The increase of aggressive interactions among robustus males provided more opportunities for typus males to seize a temporarily unguarded female. While typus males exploit fights among robustus males that produce mating opportunities for them, robustus males benefit from typus males, which reveal the presence of receptive females. We suggest that each phenotype benefits from the presence of the other phenotype and suffers costly interference among individuals of the same phenotype. Whether frequency‐dependent effects on the mating probability of subordinates also affect their ontogenetic switchpoint should be examined in future studies.     

Partial local mate competition and the sex ratio: A study on non-pollinating fig wasps

In many species, mating takes place in temporary patches where only a small number of females produce offspring. In this situation Local Mate Competition (LMC) theory predicts that the optimal sex ratio (defined as proportion males) should become increasingly female biased as the number of females contributing offspring to a patch decreases. However, in a large number of these species, some mating is also likely to occur away from the natal patch (termed partial LMC). In this case the degree of LMC is reduced, and theory predicts a relatively less female biased sex ratio. We tested these two predictions with field data from 17 species of New World non-pollinating fig wasps representing three genera. We present a model which suggests that the average number of females ovipositing in a fruit (i.e. patch) is positively correlated with the proportion of fruit of a given tree species in which that species of wasp occurs. Across species, the overall sex ratio was positively correlated with the proportion of fruit in which that species occurs. Furthermore, the males of some species are wingless, and in these species all mating must take place before females disperse from their natal fruit. In contrast, the males of other species are winged, and in these species mating may also take place away from the natal fruit. Species with winged males had less female biased sex ratios than species with wingless males that occurred in a similar proportion of fruit. Finally, the correlation between sex ratio and the proportion of fruit in which a species occurs was also observed within species when comparing between the fruit crops of different trees. This suggests that individual females facultatively adjust the sex ratio of their offspring in response to variable LMC.     

Proximate mechanisms of male morph determination in the ant Cardiocondyla obscurior

The ant genus Cardiocondyla is characterized by an extraordinary male polyphenism, with winged disperser males and wingless, territorial ergatoid males. Winged males are produced only after the colony has experienced stressful environmental conditions, e.g., a drastic temperature decrease. We investigated the proximate basis of male polyphenism and caste dimorphism in C. obscurior. The critical stage for both morph and caste determination is the end of the second of three instars. Larval development as well as duration of the pupal stage are extended both in winged males and winged females and winged reproductives need on average 8.8 days longer for the development from egg to adult than wingless ergatoid males and workers. Treatment of first and second instar larvae with methoprene, a juvenile hormone analogue, led to the expression of the winged morph, suggesting an important role of juvenile hormone in both sexes. Although queens are produced year-round in contrast to winged males, the proximate basis of variation in morphology is likely to be the same in both sexes. Whereas the larvae themselves appear to be insensitive to the environmental changes, behavioral observations revealed that workers react to stress by changing their behavior towards larvae and in this way trigger them to develop into winged males.     

钝叶榕(Ficus curtipes)非传粉小蜂交配行为

榕树及其传粉榕小蜂繁殖上相互依存,被认为是生物界中协同进化时间最悠久,相互关系最密切的一对生物;在大多数榕树种类的隐头花序内,除了传粉榕小蜂外,还共存着多种非传粉小蜂,它们的繁殖行为直接影响着榕树和传粉榕小蜂的繁殖和互惠稳定。钝叶榕(Ficus curtipes Corner),是一种雌雄同株的绞杀性榕树。研究在西双版纳热带植物园里共收集钝叶榕100个隐头果内的榕小蜂,获得9493号标本;其中,包括1种传粉小蜂和5种非传粉小蜂,钝叶榕传粉小蜂Eupristina sp.占总数的4466%,杨氏榕树金小蜂Diaziella yangi 占46.13%,而其它4种非传粉小蜂（Lipothymus sp., Sycobia sp., Philotrypesis sp.和Sycoscopter sp.）仅占9.20%。前3种榕小蜂雌蜂进到果腔产卵,其余3种在果外产卵。观测23个钝叶榕榕果出蜂情况发现,6种榕小蜂在钝叶榕隐头花序内遵循严格的羽化出蜂顺序,首先是Sycobia sp.,次之是Lipothymus sp.,再次之是杨氏榕树金小蜂,最后是钝叶榕传粉小蜂、Philotrypesis sp.和Sycoscopter sp.。5种非传粉小蜂的交配场所与雄蜂翅型无关,雄蜂有翅型的杨氏榕树金小蜂大部分交配在果内完成,而且它们的雄蜂为争夺交配机会存在激烈的打斗行为;雄蜂无翅型的Lipothymus sp.有部分雄蜂爬出隐头果,在果壁和附近的叶片背面交配;雄蜂有翅型的Sycobia sp.,其所有交配都发生在果外;Philotrypesis sp.和Sycoscopter sp. 雄蜂均无翅,它们的交配全发生在果内。局域配偶竞争使榕小蜂性比偏雌,杨氏榕树金小蜂雄蜂虽然有翅,但大部分交配发生在榕果内,这将影响其最佳的性比率。因此,依赖雄蜂翅型并不能很好地预测榕小蜂的交配场所和性比率。     

Proximate and ultimate causes of natal dispersal in the great bustard Otis tarda

Between 1991 and 1997 we studied the offspring independenceand juvenile dispersal in a wild population of great bustards(Otis tarda). Young males were independent and began their juveniledispersal at an earlier age (6–11 months) than young females(8–15 months). The juvenile dispersal period was longerand the distances reached farther in males than in females.Natal dispersal distances were also longer in males, all ofwhich dispersed from their natal areas and established as adultsat 5–65 km from their natal nests. In contrast, most femaleswere strongly philopatric, settling at 0.5–5 km from theirnatal nests. These marked sex differences in offspring independenceand dispersal may have evolved originally to maintain geneticdiversity and are probably reinforced through male competitionfor mates. Young males that had fed at higher rates and receivedmore feedings from their mothers during the early maternal dependenceperiod became indepthdent and tended to disperse earlier. Theyalso integrated earlier into adult male flocks and settled earlierat their definitive leks, which were closer to their natal sites,in areas of higher adult male density. None of these correlationswas found among young females. These results suggest that enhancedfood intake and maternal care of male offspring are vitallyimportant in increasing their competitive ability during theimmature period and probably also in their fitness as breedingadults. These results are in accordance with the selective valueof large size in males and suggest how this species might havereached such a marked sexual dimorphism in size.     

Is offspring dispersal related to male mating status? An experiment with the facultatively polygynous spotless starling

Patterns of natal dispersal are generally sex‐biased in vertebrates, i.e. female‐biased in birds and male‐biased in mammals. Interphyletic comparisons in mammals suggest that male‐biased dispersal occurs in polygynous and promiscuous species where local mate competition among males exceeds local resource competition among females. However, few studies have analysed sex‐biased patterns of dispersal at the individual level, and facultatively polygynous species might offer this opportunity. In the spotless starling, polygynous males exhibit their mating status during courtship carrying higher amounts of green plants to nests than monogamous males. We experimentally incorporated green plants to nests during four years to analyse long‐term consequences on breeding success and offspring recruitment rates. We unexpectedly found that experimental sons recruited farther than experimental daughters, while control daughters recruited farther than control sons. A similar pattern was found using observational information from eight years. We discuss this result in the context of local competition hypothesis and speculate that sons dispersed farther from nests controlled by polygynous males to avoid competition with relatives. The amount of green plants in nests affects female perception of male attractiveness and degree of polygyny, although little is known about proximate mechanisms linking this process with the offspring dispersal behaviour. Our results support the idea that male‐biased dispersal is related to polygyny in a facultatively polygynous bird.     

Mating‐Associated Changes in the Behaviour of Leptothorax gredleri Ant Queens

Throughout their lives, animals adapt their behaviour to environmental fluctuations and to their own requirements. In social insects, behavioural changes are often particularly conspicuous. For example, in many ant species, reproductive sexuals leave their maternal nests and engage in risky mating and dispersal activities. Female sexuals experience, during a short period of time, dramatic changes in terms of behaviour and environmental conditions. But because sexual activities of ants are not easily observed, few studies have quantified in detail how behaviour alters with maturation and mating. We studied how various behavioural traits of Leptothorax gredleri female sexuals, a species in which female sexuals attract males by ‘female calling’, change before and after mating. We tested the hypothesis that behavioural variation reflects the altered requirements of queens to adapt to a particular situation. To this end, we compared geotactic, phototactic and locomotor behaviour across a wide range of life stages from lightly coloured, unmated female sexuals to old, mated queens. The results showed that female sexuals of L. gredleri change conspicuously their geotactic, phototactic and locomotor behavioural traits over their life stages. Three different behavioural states were evident (1) from light to dark female sexuals, individuals have negative phototaxis and reduced locomotor activity; (2) mature female sexuals during the daily period of sexual activity have strong phototaxis, negative geotaxis and an important locomotor activity; and (3) freshly mated and old mated queens avoid light and decrease their locomotor activity. These sharp differences in behaviour between stages match the transition from the relative safety of the nest chamber to the adversary world outside the nest , and back.     

Age‐dependent male mating tactics in a spider mite—A life‐history perspective

Males often fight with rival males for access to females. However, some males display nonfighting tactics such as sneaking, satellite behavior, or female mimicking. When these mating tactics comprise a conditional strategy, they are often thought to be explained by resource holding potential (RHP), that is, nonfighting tactics are displayed by less competitive males who are more likely to lose a fight. The alternative mating tactics, however, can also be explained by life‐history theory, which predicts that young males avoid fighting, regardless of their RHP, if it pays off to wait for future reproduction. Here, we test whether the sneaking tactic displayed by young males of the two‐spotted spider mite can be explained by life‐history theory. We tested whether young sneaker males survive longer than young fighter males after a bout of mild or strong competition with old fighter males. We also investigated whether old males have a more protective outer skin—a possible proxy for RHP—by measuring cuticle hardness and elasticity using nanoindentation. We found that young sneaker males survived longer than young fighter males after mild male competition. This difference was not found after strong male competition, which suggests that induction of sneaking tactic is affected by male density. Hardness and elasticity of the skin did not vary with male age. Given that earlier work could also not detect morphometric differences between fighter and sneaker males, we conclude that there is no apparent increase in RHP with age in the mite and age‐dependent male mating tactics in the mite can be explained only by life‐history theory. Because it is likely that fighting incurs a survival cost, age‐dependent alternative mating tactics may be explained by life‐history theory in many species when reproduction of old males is a significant factor in fitness.     

Macro- and microgeographic genetic structure in an ant species with alternative reproductive tactics in sexuals

The genetic structure of social insect populations is influenced by their social organization and dispersal modes. The ant Hypoponera opacior shows diverse reproductive behaviours with regular cycles of outbreeding via winged sexuals and inbreeding via within-nest mating wingless sexuals that reproduce by budding. This unusual life cycle should be reflected in the genetic population structure, and we studied this on different scales using microsatellites. On a macrogeographic scale, populations were considerably structured and migration rates within the Chiricahuas were higher than those in between mountain ranges. On a local scale, our analyses revealed population viscosity through dependent colony foundation and a high genetic diversity with a multicolonial structure. The latter was also evident from recognition trials revealing consistent aggression between non-nestmates. Within-nest matings led to high inbreeding coefficients. Finally, the observed seasonal changes in relatedness can be explained by variation in queen number and differential dispersal of the two reproductive morphs.     

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.