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Measuring reproductive costs is crucial to understanding sexual conflict and its evolutionary outcomes. Sexual conflict is thought to originate from anisogamy—the size difference between male and female gametes; if sperm are tiny and not produced in vastly greater numbers than eggs, at any mating females’ gametic investment is larger than that of males. Testing this prediction has proven difficult, especially because males and females differ in many more traits than just gamete size. We overcame this difficulty by exposing simultaneously hermaphroditic polychaete worms Ophryotrocha diadema (two sexual functions in the same body) to two social conditions, pairs, and groups >2, where hermaphrodites invest either relatively more in the female function or relatively more in the male function, respectively. Then we measured four markers of cellular oxidative status, a physiological mediator of life-history strategies. Less female-biased hermaphrodites produced fewer eggs but, unexpectedly, had lower levels of antioxidant protection than more female-biased hermaphrodites, which produced more eggs. Male-biased hermaphrodites compete for mating as males (hermaphrodites in pairs do not) suggesting that in the short-term male competition might be costlier than egg production in terms of regulation of oxidative status. These results highlight the need of including behavioral traits, namely competition over egg fertilization, in the measures of reproductive costs.

Traditionally, dominant breeders have been considered able to control other individuals’ reproduction in multi-member groups with high variance in reproductive success/reproductive skew (e.g., forced sterility on subordinate conspecifics in eusocial animals; suppression of sex change in sequential hermaphrodites). These actions are typically presented as active impositions by reproductively dominant individuals. However, how can individuals regulate the physiological reproductive state of others? Alternatively, less reproductively successful individuals could self-restrain from reproduction in presence of dominant breeders. Shifting perspective from a top-down manipulation to a broader view (which includes all contestants) and using a multi-taxa approach, we propose a resolution of reproductive-skew conflicts based on signalling rather than control, along a continuum of levels of strategic regulation of reproduction.

Social insects communicate by using chemical, visual, tactile, and acoustic signals, including stridulations. Ectatomma ruidum is a mainly Neotropical ant species complex that has faced strong divergence at the genetic level; the species have a highly variable blend of cuticular hydrocarbons and a relatively conserved morphology. Based on evidence for genetic and chemical differentiation, we tested for variation in acoustic traits. We compared the stridulations produced by the species E. ruidum sp. 2, sp. 3–4 and the new putative species E. ruidum sp. 5, as well as the morphology of the stridulatory file. We found that the stridulations produced by E. ruidum sp. 5 were statistically different from those of the other species in a number of traits. The differences in stridulatory traits might rely more on the way the ants produce the sound (rubbed area percentages) than on the morphology of the stridulatory file, for which we did not find variation. Our results highlight the use of acoustic traits as potential taxonomic tools for integrative taxonomic studies and suggest that the acoustic traits of E. ruidum species complex have been subjected to selection.

Conditional reciprocity (help someone who helped you before) explains the evolution of cooperation among unrelated individuals who take turns helping each other. Reciprocity is vulnerable to exploitations, and players are expected to identify uncooperative partners who do not return the help they received. We tested this prediction in the simultaneously hermaphroditic worm, Ophryotrocha diadema, which engages in mutual egg donations by alternating sexual roles (one worm releases’ eggs and the other fertilizes them). We set up dyads with different cooperativeness expectations; partners were either the same or a different body size (body size predicts clutch size). Large worms offered larger clutches and did so sooner when paired with large rather than small partners. They also released smaller egg clutches when they started egg donations than when they responded to a partners’ donation, fulfilling the prediction that a players’ first move will be prudent. Finally, behavioral bodily interactions were more frequent between more size-dissimilar worms, suggesting that worms engaged in low-cost behavioral exchanges before investing in such costly moves as egg donations. These results support the hypothesis that simultaneously hermaphroditic worms follow a conditional reciprocity paradigm and solve the conflict over sexual roles by sharing the costs of reproduction via the male and the female functions.

In social wasps, female lifespan depends on caste and colony tasks: workers usually live a few weeks while queens as long as 1 year. Polistes dominula paper wasps infected by the strepsipteran parasite Xenos vesparum avoid all colony tasks, cluster on vegetation where parasite dispersal and mating occur, hibernate and infect the next generation of wasp larvae. Here, we compared the survival rate of infected and uninfected wasp workers. Workers’ survival was significantly affected by parasite sex: two-third of workers parasitized by a X. vesparum female survived and overwintered like future queens did, while all workers infected by a X. vesparum male died during the summer, like uninfected workers that we used as controls. We measured a set of host and parasite traits possibly associated with the observed lifespan extension. Infected overwintering workers had larger fat bodies than infected workers that died in the summer, but they had similar body size and ovary development. Furthermore, we recorded a positive correlation between parasite and host body sizes. We hypothesize that the manipulation of worker’s longevity operated by X. vesparum enhances parasite’s fitness: if workers infected by a female overwinter, they can spread infective parasite larvae in the spring like parasitized gynes do, thus contributing to parasite transmission.

In outcrossing hermaphrodites with unilateral mating, where for each mating interaction one individual assumes the female role and the other the male role, each individual must take a sexual role opposite to that of its partner. In the polychaete wormOphryotrocha diadema, the decision on sexual role is likely at stake during the day-long courtship. Here we describe, for the first time, courtship and pseudocopulation in this species, quantify their pre-copulatory behavior, and search for behavioral traits predicting the prospective sexual role (i.e., behavioral sexual dimorphism), by analyzing the courtship behavior of pairs of worms during the day preceding a mating event. We did not find any behavioral cue predicting the sexual role worms were to play; partners’ pre-copulatory behaviors were qualitatively and quantitatively symmetrical. We interpret this as the outcome of a war of attrition where partners share the preference for the same sexual role, and both hide their ‘willingness’ to play the less preferred one, until one individual reaches its cost threshold and accepts the less preferred sexual role.

Reproductive traits are often tightly linked to variations in the social environment. In animals with separate sexes, producing male or female offspring results in different fitness gains depending on population structure. In simultaneous hermaphrodites, allocating a given proportion of resources to the two sexes results in fitness gains that depend on mating opportunities, and extremely plastic hermaphrodites may have a selective advantage. To test to what extent hermaphrodites have flexible and reversible sex allocation at the individual level, we exposed hermaphroditic Ophryotrocha diadema worms (an obligatorily nonselfing polychaete, with low numbers of aflagellate, immotile sperm and ‘pseudocopulation’) to weekly changes in actual or simulated mating opportunities and mate competition (controlling for density effects). We found that worms rapidly switched from high investment in the female function (eggs and courting) to high investment in the male function (aggressive behaviour) with increasing mating opportunities. Simulated mate competition and competition over the male role triggered similar variations in egg production (i.e. worms laid fewer eggs), indicating that these worms preferred to mate in the male role. These results highlight the key role of behaviour in the study of reproductive investment in hermaphrodites and the importance of plasticity in sex allocation (including precopulatory behaviours) in hermaphrodites as a way to compete for the male role and to keep hermaphroditism stable in fluctuating environments.

International audience; In social insects, chemical communication is the main communication mode among colony members, which use the blends of cuticular hydrocarbons as recognition cues to discriminate between nestmates and non-nestmates and to prevent the exploitation of their nest resources by aliens. The aim of this study was to assess the variation of nestmate recognition cues in the ant Ectatomma ruidum, a species complex with a considerably conserved morphology and one of the few ant species where intraspecific thievery, a form of cleptoparasitism, has been reported. We analyzed the cuticular hydrocarbon profiles of ants collected from a number of geographically separated populations, and examined DNA sequence data to assess their species identity. We focused on one species of the complex, E. ruidum sp. 3-4, whose species delineation remains controversial. We documented that several quantitative and qualitative traits of the cuticular hydrocarbon profiles varied significantly between populations, indicating that this species harbors more cuticular chemical phenotypic diversity than expected within a single species. In particular, there was a striking divergence among populations in the proportion of methylalkanes, alkenes, alkadienes and odd-chain components, which likely play a major role in nestmate/non-nestmate discrimination, a process which might have been crucial in these cleptobiotic ants. Further investigations are needed to test the hypothesis that biotic pressures, such as the need to discriminate conspecific intruders and limit thievery, could have played an important role in promoting the evolutionary divergence between populations in this ant species complex.

Simple Summary The co-evolution of hosts and parasites depends on their ability to adapt to each other's defense and counter-defense mechanisms. The strength of selection on those mechanisms may vary among populations, resulting in a geographical mosaic of co-evolution. The boreo-montane paper wasp Polistes biglumis and its parasite Polistes atrimandibularis exemplify this type of co-evolutionary system. Here, we used genetic markers to examine the genetic population structures of these wasps in the western Alps. We found that both host and parasite populations displayed similar levels of genetic variation. In the host species, populations located near to each other were genetically similar; in both the host and the parasite species populations farther apart were significantly different. Thus, apparent dispersal barriers (i.e., high mountains) did not seem to restrict gene flow across populations as expected. Furthermore, there were no major differences in gene flow between the two species, perhaps because P. atrimandibularis parasitizes both alpine and lowland host species and annually migrates between alpine and lowland populations. The presence of strong gene flow in a system where local populations experience variable levels of selection pressure challenges the classical hypothesis that restricted gene flow is required for local adaptations to evolve. The co-evolutionary pathways followed by hosts and parasites strongly depend on the adaptive potential of antagonists and its underlying genetic architecture. Geographically structured populations of interacting species often experience local differences in the strength of reciprocal selection pressures, which can result in a geographic mosaic of co-evolution. One example of such a system is the boreo-montane social wasp Polistes biglumis and its social parasite Polistes atrimandibularis, which have evolved local defense and counter-defense mechanisms to match their antagonist. In this work, we study spatial genetic structure of P. biglumis and P. atrimandibularis populations at local and regional scales in the Alps, by using nuclear markers (DNA microsatellites, AFLP) and mitochondrial sequences. Both the host and the parasite populations harbored similar amounts of genetic variation. Host populations were not genetically structured at the local scale, but geographic regions were significantly differentiated from each other in both the host and the parasite in all markers. The net dispersal inferred from genetic differentiation was similar in the host and the parasite, which may be due to the annual migration pattern of the parasites between alpine and lowland populations. Thus, the apparent dispersal barriers (i.e., high mountains) do not restrict gene flow as expected and there are no important gene flow differences between the species, which contradict the hypothesis that restricted gene flow is required for local adaptations to evolve.

In the paper wasp Polistes dominula, cuticular hydrocarbons play a critical role to acquire information regarding conspecific individuals. However, the relationship between cuticular hydrocarbons, health status, and male sexually selected traits is poorly investigated. In this study, we characterized the cuticular hydrocarbon profile of adult male and female wasps, infected or not by the strepsipteran endoparasite Xenos vesparum, to assess whether the chemical signature provides information about sex and health status (parasite infection). Moreover, we tested whether the chemical profile reflects male quality as measured via morphological and behavioural (sexually selected) traits at leks. Our results showed that males and females had similar total amount of CHCs, quantitatively different profiles and, to a lesser extent, sex-specific chemical compounds. Cuticular profiles were influenced by the strepsipteran infection, and the effect was stronger in females (the primary host) than in males, according to the physiological castration of female but not of male hosts. Regarding territorial and non-territorial males, no significant difference emerged in their chemical profiles. Furthermore, sex-dimorphic visual signals (size, shape, and asymmetry of abdominal yellow spots) were related to the behavioural displays of territorial males. We hypothesize that cuticular hydrocarbons are potential multi-role cues to assess sex and health status in male and female wasps, in synergy with visual signals and territorial performance in signaling male quality.

Brood and social parasites exploit the parental care of their host and often integrate into host colonies using different strategies at different moments during their life cycle. In social wasps, the obligate social parasite Polistes atrimandibularis, using chemical mimicry and chemical insignificance, avoids detection by its host, Polistes biglumis, which has an efficient nestmate recognition system. Enslaved host foundresses accept and care for parasite brood as if it were their own. This observation raises the following question: how exactly do parasite brood escape detection and increase host acceptance? Here, we compared the cuticular chemical signatures of parasite brood and host brood. Their signatures differed in composition: parasite larvae and pupae had particularly high levels of alkenes (notably 9-nonacosene), which were absent in host larvae and pupae. Given this result, we tested the effect of 9-nonacosene on host foundresses, and documented that they reduced their aggression. Our findings address a novel integration strategy for social parasite brood as they suggest that the hydrocarbon serves as an appeasement substance and promotes host tolerance of parasite larvae and pupae, which are chemically disparate from host larvae and pupae.

In complex societies, communication signals function as fine tools for regulating social structure and coordinating activities, while enabling groups to adjust their strategies flexibly in response to ecological conditions. Social wasps of the genus Polistes perform vibratory movements, which are expressed by dominant individuals mainly during adult-larva feeding interactions. Recent investigations have hypothesized that these signals may influence caste differentiation during larval development. We tested this hypothesis by conducting behavioural observations in the field, in three populations of social wasps (Polistes biglumis) differing in caste ratio: In some populations, foundresses produce workers and future reproductives; in others, workers are rarely produced. We observed that only foundresses produced vibratory signals, which were expressed during larval feeding sessions and only in the period before offspring emergence. Foundresses belonging to populations with workers spent more time producing vibratory signals than those from populations where workers are rare. In some populations, social parasites invaded colonies and subdued host foundresses. Subdued foundresses produced fewer vibratory signals than foundresses of unparasitized colonies. Our data suggest that the dominant status is necessary for the expression of vibratory signals and show that foundresses from different populations produced different numbers of vibratory signals. This difference can be explained well by the hypothesis that vibratory signals influence larval development and promote the production of workers. We suggest that these signals may have been the target of selective forces, in order to regulate caste ratio and maximize colony fitness under local conditions.

Polychaetes (i.e. non-clitellate annelids) display one of the highest diversities of reproductive traits among marine invertebrates, due to the wide variety of habitats they have colonized and the relative simplicity of their reproductive system. Among polychaetes (i.e. non-clitellate annelids), the genus Ophryotrocha is one of the best-studied models in sexual system investigations and is providing several clues as to how the evolutionary transition from hermaphroditism to gonochorism may have occurred. Within the genus, there are both hermaphroditic and gonochoric species, but many species exhibit traits intermediate between the two sexual systems. Hermaphroditic species are able to plastically adjust their sex allocation to current mating opportunities, by diminishing the proportion of resources invested into the female function and increasing those invested into the male function, when mating opportunities increase (although the enhanced investment in the male function is expressed in behavioural traits—such as mate competition—rather than increased sperm production). Occasionally, hermaphrodites specialized in the male function are found in hermaphroditic populations (functional-male hermaphrodites), which might represent a first step towards gender specialization. On the other hand, multiple sexual phenotypes have been described in gonochoric (sexually dimorphic) species, with males which produce oocytes and females which produce sperm, which are likely to be vestigial hermaphroditic traits. The existence of functional-male hermaphrodites in hermaphroditic populations and of males and females which produce both eggs and sperm in gonochoric species suggest that in Ophryotrocha the transition from hermaphroditism to gonochorism occurred via androdioecy, that is, through an evolutionary trajectory involving an intermediate stage where both hermaphrodites and males are present.

Nestmate recognition codes show remarkable chemical complexity, involving multiple biochemical pathways. This complexity provides the opportunity to evaluate the ecological and social conditions that favor the evolution of complex signaling. We investigated how the chemical signatures of three populations of the social paper wasp Polistes biglumis differed in terms of concentration of hydrocarbons, proportions of branched hydrocarbons and overall variation. We tested whether the variation in chemical signatures among populations could be explained by the prevalence of social parasites or whether this was just an effect of local abiotic conditions which influenced the composition of the hydrocarbon cuticular layer. We studied the chemical signa- ture in three populations in which obligate social parasites differed in the selection pressures they imposed on host populations. Within each population, we restricted our analyses to non-parasitized hosts, to avoid potential short-term effects of parasite pres- ence on the host chemical signatures. We found that host colonies in parasitized populations had more diverse profiles than the parasite-free population. Moreover, the overall concentration of hydrocarbons and the relative proportion of branched hydrocar- bons were larger in the parasitized populations, relative to the non-parasitized one. This is to our knowledge the first evidence in favour of the hypothesis that different traits in the host chemical signatures as a whole undergo evolutionary changes resulting from directional or balancing selection imposed by social parasites. We conclude that obligate social parasites act as 'engines of diversity' on host chemical signatures and operate in favor of a geographic mosaic of diverging communication codes (Current Zoology 60 (1): 137148, 2014). Keywords Polistes, Brood parasitism, Cipher, Nestmate recognition, Hydrocarbons, Geographic mosaic, Crozier's paradox

In animals in which the two sexes invest relatively similar amounts of resources in their young, the number of mates is expected to affect male and female reproductive success similarly and gender conflicts on the number of mates may not arise. Correspondingly, in non-selfing, simultaneous hermaphrodites with long-term monogamy, the two partners are expected to alternate repeatedly their sexual roles and invest similarly in their offspring. Therefore, the gender conflict on the number of mating partners should not arise. However, when >2 conspecifics are present, hermaphrodites are known to plastically adjust their behavior and sex allocation and compete for mating repeatedly in the male role. We tested whether this leads to multiple paternities of single egg clutches in experimental replicates of small and large groups of non-selfing, egg-trading, behaviorally monogamous polychaete worms (Ophryotrocha diadema) by using neutral genetic markers to estimate paternity. Multiply fertilized egg cocoons were common in these worms; two or more individuals succeeded in fertilizing the same egg cocoon and mate competition increased with group size. Multiply fertilized egg cocoons had a higher proportion of eggs developing into mature worms than singly fertilized egg cocoons. Possibly singly fertilized cocoons had a lower fertilization rate owing to low sperm counts and aflagellate sperm.

Phenotypic plasticity is the environment-induced change in the phenotype of an organism. Natural selection operates for the ability of individuals to adjust their phenotype to the current environmental conditions when environmental conditions fluctuate. Simultaneous hermaphrodites may exhibit plasticity in sex allocation according to the availability of mates at any particular time. The plasticity in sex allocation has probably evolved under fluctuating mating opportunities, which are usually low but increase when hermaphrodites incur sudden demographic expansion. Here we compare the plasticity in sex allocation in two different populations of the hermaphroditic polychaete worm Ophryotrocha diadema – a laboratory population and a wild one. Worms from the laboratory population were kept under constant crowded conditions for about 200 generations (i.e. they were exposed to high mating opportunities). Worms from the wild population were kept under crowded conditions for 20 generations only. Worms fr...

We used DNA microsatellites to study colony kin structure and breeding patterns in the primitively eusocial wasp Polistes biglumis. P. biglumis inhabits cool areas at high altitudes and, as a consequence, has a reduced colony cycle compared to more temperate Polistes. P. biglumis colonies are always founded and controlled by a single foundress, but nest failure is common and foundresses losing their nests do not have time to start new ones due to the short season. Instead, nests are characterized by frequent female turnover, in the form of females taking over (usurpation) other con-specific nests. Our results showed that most nests had offspring from multiple unrelated females, including some where multiple females were not observed in monitoring. Reconstruction of behavioural events from the genetic data revealed three types of multiple matriline nests: (a) nests that were usurped by another female, where the original nest owner disappeared following the usurpation event, (b) nests that were joined by another female, where the original nest owner stayed following the joining event, (c) nests that were both usurped and joined by other females. We also found, for the first time, a clear indication of multiple mating by Polistes females. Moreover, males mating with the same female were related, which may be explained by the lek mating system of P. biglumis. Finally, we analysed the nest sex ratios and how it changed during the season and found that sexes were produced sequentially, males before females.

Summary Reciprocity [ 1 ] is one of the most controversial evolutionary explanations of cooperation among non-kin [ 2 , 3 ]. For some authors, cognitive capacity of non-human organisms is limiting, and more parsimonious mechanisms should apply [ 3 , 4 , 5 ]; for others, the debate is mainly semantic [ 2 , 6 ], and empirical evidence can be found in a wide range of taxa [ 7 ]. However, while the ability to alternate cooperative behaviors does not settle the reciprocity controversy, the capacity to adjust cooperative behavior to the value of received help could prove decisive. Marine polychaete worms Ophryotrocha diadema, as several simultaneous hermaphrodites, do not self-fertilize and have unilateral mating (i.e., they behave either as females or as males during each mating event). They are also external fertilizers and thus cannot store allosperm, which contribute to make them ideal model organisms to investigate reciprocity, since partners usually alternate sexual roles with each other, repeatedly exchanging egg clutch of variable size [ 8 , 9 , 10 , 11 , 12 ]. However, whether the alternation of sexual roles is the result of conditional reciprocity rather than by-product reciprocity has never been tested [ 13 ]. Here, we show that O. diadema worms reciprocate eggs conditionally to the partner’s behavior and adjust the quality of cooperation according to that of their partners. Moreover, only egg reciprocation offers similar fitness returns via both the female and the male function with respect to non-reciprocating laying strategies. These results document that fine-tuned forms of conditional reciprocity can emerge in cognitively unsophisticated animals, broadening the criteria to recognize conditional reciprocity among animals.

In the mating system of simultaneously hermaphroditic animals, sexual allocation is predicted to vary as a function of the number of potential mates. According to the Hermaphrodite's Dilemma, sexual conflict over the preferred sexual role in hermaphroditic animals is resolved by reciprocity (i.e. by alternating sexual roles), accompanied by the animals' occasional cheating in the preferred role at a relatively low frequency. In a 350-generation-old laboratory strain of the pair-mating outcrossing hermaphroditic polychaete worm Ophryotrocha diadema, we show that 9% of the individuals mated only in the male role over long periods, indicating a male-role preference (temporary functional males). Furthermore, 2% of the individuals mated for their whole lifetime exclusively as males (permanent functional males). These findings indicate that the sex allocation of some individuals may vary from the predicted optimal sex allocation for the population. Morphologically, functional males exhibited a hermaphroditic phenotype (i.e. they matured a single batch of oocytes that they never laid and acted as functional males). We show that temporary functional males appeared in hermaphroditic populations under promiscuous mating regimes significantly more often than under monogamous ones. Indeed, under promiscuity, there are many mating opportunities and O. diadema hermaphrodites compete for mates, whereas, under monogamy, the two partners regularly take turns in laying cocoons and fertilizing their partner's cocoon. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100, 451–456.

Sulcopolistes atrimandibularis Zimmermann is the obligate social parasite of Polistes biglumis bimaculatus Geoffry in Furcroy, a mountain species of paper wasp. Unlike all the other hymenopteran social parasites, the Sulcopolistes female obtains part of the food for her immature brood by plundering other nests of the host species. Parasite females can control more than one host nest: one of them (the nursery nest) she uses solely for reproduction purposes (from which the Sulcopolistes reproductives emerge) and others (supply nests) are used for exploiting the Polistes brood content. It is possible that this behaviour is an adaptation to the extremely short colonial cycle of the host.

In primitively eusocial insects, caste expression is flexible. Even though Polistes species are well known to show social trait variation (e.g., worker vs. gyne) depending on ecological context, loss of worker caste in some populations of a eusocial, worker-containing species has never been documented. We report first data on geographic variation in caste expression in Polistes biglumis. We compared physiological and behavioural traits of the first female offspring from four populations that experience different climatic conditions and social parasite prevalence. We demonstrated that the first female offspring to emerge in cold areas with high parasite prevalence had more abundant, gyne-like fat bodies and exhibited lower foraging effort, in comparison to the first female offspring produced in warm areas with low parasite prevalence. Thus, the populations under severe environmental conditions produced a totipotent female offspring and suppressed worker production, whereas the population living in less extreme environmental conditions produced worker-like females as first female offspring and gyne-like females as offspring that emerged later. The existence of mixed social strategies among populations of primitively eusocial species could have important consequences for the study of social evolution, shedding light on the sequence of steps by which populations evolve between the extremes of solitary state and eusocial state.

The role of sexual selection in shaping the mating system of hermaphrodites is currently widely accepted. However, a quantification of the intensity of sexual selection in hermaphroditic animals has never been accomplished. We evaluated the opportunity for sexual selection for both the female and the male functions in the simultaneous outcrossing hermaphrodite Ophryotrocha diadema by measuring focal hermaphrodites' paternal and maternal offspring in experimental replicated monogamous and promiscuous populations, using genetic markers to estimate paternity. Opportunity for sexual selection for each of the two sexual functions was quantified by means of the Crow's index, i.e. the ratio of variance in progeny number to the squared mean number of progeny. In addition, the extent to which the reproductive success was shared among competing individuals was estimated by means of the Nonacs's B index. We documented that the strength of selection on the male and female function in hermaphrodites with external fertilization depends on the reproductive context. Under a promiscuous regime, hermaphrodites have higher opportunities for selection for both the male and the female function than under the monogamous regime. Moreover, the reproductive skew for the female function becomes greater than that for the male function, moving from monogamy to promiscuity. In our model system, allocation to one sexual function is opposed by any degree of allocation to the other, indicating that sex-specific patterns of selection operate in this model species.

Polistes foundresses can behave as facultative social parasites when, instead of founding their own nest, they usurp colonies of the same or a different species and temporary use the host workforce to raise their own brood. Conspecific usurpation appears to be common among Polistes wasps, but nothing is known about the mechanisms that these facultative social parasites use to have themselves accepted within usurped colonies. Using behavioural tests, we studied the chemical strategies employed by females of Polistes nimphus when they behave as facultative social parasites in colonies of the same or of a different species. We hypothesized that usurpers would mark host nests with their own odours and/or acquire host nest odours in order to camouflage their real identity from host workers. Our results indicated that P. nimphus usurpers used different chemical strategies depending on host nest species: they acquired conspecific host odours but marked heterospecific host combs with their own odours. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91, 505–512.

One of the greatest remaining problems in the field of sex allocation is the variation across species of the extent to which individuals adjust their offspring sex ratio or sex allocation according to environmental conditions. Particularly in the field of sex allocation, there is a lack of research on the mechanisms and cues involved. We address this problem in the outcrossing simultaneous hermaphroditic polychaete Ophryotrocha diadema, which shifts sex allocation by suppressing the female function in the presence of reproductive competitors or multiple partners. We document that O. diadema hermaphrodites can evaluate group size by means of a species-specific chemical released by mature individuals in water. The perception of such a water-borne signal is sufficient to trigger the observed shift in sex allocation, i.e., a suppression of the female function, irrespective of the frequency of encounters with conspecifics. Under natural conditions, such a pheromone will favor partners' encounters and the adjustment of individual sex allocation according to the numbers of reproductive competitors and/or potential partners. Copyright 2006.

Sex allocation theory predicts that simultaneous hermaphrodites shift sex allocation facultatively in response to variation in local group size. This study was performed to evaluate the relative investment in each sex function by the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema and to test whether allocation to each sex depends on the number of reproductive competitors. Four experimental groups were set up (in a 2 · 2 factorial design) with small or large group size and with small or large enclosures to control for potential confounding effects of density. We measured the proportion of female and male investment in focal individuals. Results revealed that individuals regulated their reproductive output so that when reproductive competitors were present, the number of female gametes was strongly reduced and the male function increased. In contrast, under monogamy, individuals in small groups produced lower numbers of sperm but had a higher egg output than worms in large groups. Density did not affect sex allocation in our experiment. Our findings provide qualitative support for Local Mate Competition theory, but also show that the pattern of sex allocation specific to this species is more complex than expected by current theory.

Chemical cues are so important in the recognition mechanism of social insects that most social parasites (which rely on hosts to rear their brood) have been documented as overcoming the mechanism by which colony residents recognize non-nestmates, by mimicking the odour of the usurped colony. We simulated in the laboratory the process by which the obligate social parasite, Polistes semenowi, invades nests of the host species, Polistes dominulus, in the field and analysed the epicuticular lipid layer before and after host nest usurpation. The experiment documents that P. semenowi social parasites have an epicuticular hydrocarbon pattern which is very similar to that of their host but, after entering host colonies, parasites mimic the odour of the colonies they invade, to the point that they perfectly match the hydrocarbon profile peculiar to the colony they entered. However, both before and after host nest invasion, parasites show a tendency to possess diluted recognition cues with respect to their hosts.

Queens of the parasitic social wasp, Polistes atrimandibularis, temporarily mimic the odor of their host species, Polistes biglumis, but their offspring have parasite-specific odors. As a consequence, in parasitized colonies individuals with different odors co-inhabit the colony and host workers, who are responsible for colony defense, accept wasps with different odors. In order to verify whether this particular condition causes a change in recognition abilities of hosts, we tested nestmate/non-nestmate discrimination in field colonies invaded by social parasites (and in non-parasitized colonies as controls). Results show that parasitized colonies distinguish between nestmates and non-nestmates, distinguish their parasite queen from those that usurped alien colonies, and accept their parasite's non-mimetic offspring but make more recognition errors than non-parasitized colonies. The optimal acceptance threshold model predicts that when the frequency of encountering non-kin increases, residents become less permissive towards intruders. However, my data show that parasitized colonies are more permissive towards non-nestmates with respect to non-parasitized colonies but they are also more aggressive towards nestmates, suggesting that host workers' learning abilities are impaired.

Sex allocation theory for simultaneous hermaphrodites predicts that hermaphrodites have a fixed amount of reproductive resources to allocate to both sex functions and that they trade off their allocation to both sexes depending on environmental conditions. Ophryotrocha diadema is a simultaneous hermaphroditic polychaete worm which has a protandrous phase prior to the hermaphroditic phase. The ability of adolescent males to compete with mature hermaphrodites for egg fertilization and the costs of an increase in male expenditure during the protandrous phase were tested in experiments where adolescent males had the possibility to fertilize hermaphrodites’ eggs. Results document that adolescent males were able to compete with hermaphrodites for egg fertilization and caused the hermaphrodites fitness losses of 31.4%. Adolescent males which fertilized hermaphrodites’ eggs had a slower growth rate than males which had no possibility to fertilize eggs. This result indicates that an increased male expenditure is a cost for adolescent males and that, during the protandrous phase, resources are allocated to reproduction at the expense of somatic development. © 2003 The Linnean Society of London. Biological Journal of the Linnean Society , 2003, 78, 149–154.

International audience; Nestmate recognition is a common phenomenon insocial insects that typically is mediated by cuticular hydrocarbons.Geographical variation in cuticular hydrocarbons hasbeen observed, although the pattern of variation is not consistentacross species and is usually related to the biology andecology of the different species. Polistes biglumis(Hymenoptera: Vespidae) is a social wasp that lives in highmountains where populations are separated by significantgeographical barriers. Here we investigated the level of chemicalvariation among populations of P. biglumis in the Alps,and shed light on the phylogeography of this species.Populations could be discriminated bymeans of their cuticularhydrocarbon profiles, which showed a pattern consistent withthe isolation-by-distance hypothesis. Molecular datahighlighted two areas with different levels of haplotype diversity,although all wasps belonged to the same species. Theseresults suggest that the populations of P. biglumis in the Alpsare geographically isolated from one another, favoring theirgenetic and chemical differentiation.

Sex allocation theory assumes that male and female reproductive functions share a common limited resource pool and are negatively correlated in hermaphrodites. Here we report on the first artificial selection experiment designed to test the existence of genetically-based correlations between sex functions in hermaphroditic animals. The polychaete worm Ophryotrocha diadema has a long juvenile male phase, and then shifts to the simultaneously hermaphroditic phase. We selected two sets of lines of worms for a short male phase and, after four generations, worms had a significantly shorter male phase than their generation-0 ancestors. As negatively correlated responses, generation-4 worms spent more time maturing eggs and produced a higher number of eggs at 1st laying than worms of generation 0. Both traits contributed to the female function and were not the target of the selection experiment. In contrast, selection was ineffective in the lines descending from phenotypically-hermaphroditic worms that reproduce...

Social recognition has rarely received attention in the studies on annelids. This is not surprising since the biology of behavioral interactions in annelids is mostly unexplored. Only few pheromones have been identified, which function as cues in mate recognition and gamete release. Many annelids use chemical and visual cues to locate partners and classify them according to mating status, body size, or oocyte ripeness. In some hermaphroditic polychaete worms and leeches the ability to recognize the quality of potential partners seem to be very refined, especially in relation to the ability to assess the number of competitors over mating. These examples suggest that sexual selection might have favored individual ability to assess conspecific numerosity accurately and vary their male and female resource allocation (sex allocation) accordingly. Finally, annelids can estimate whether they are related to their potential partners and whether they belong to the same or a different population, which again result in adjustments of their reproductive allocation. We suggest that sexual selection is likely to be responsible for the evolution of the ability to assess mate quality and social group size because sex allocation adjustments are favored by sexual selection.

Labile sex expression is considered to play a key role in the evolution of breeding systems and in the transition from hermaphroditism to dioecy, according to the evolutionary models proposed for plants. While in hermaphrodites sex allocation within the individual can be plastically adjusted in response to social environment, in dioecious species it is predicted to be fixed. However, labile sex expression in the form of gender plasticity can still be present in dioecious species of animals with environmental sex determination. It is still unclear how gender plasticity is involved in the evolution of breeding systems and what its role is in the transition from hermaphroditism to dioecy. We assessed the degree of plasticity in gender expression in three dioecious species of polychaete worms of the genus Ophryotrocha. We found sexual polymorphism and plasticity in sex expression during the juvenile phase to be a response to social environment. The majority of juveniles reared with an adult female or male expressed the gender opposite of that of the partner, so as to form heterosexual pairs. On the basis of these findings we outline a possible evolutionary pathway of the transition from hermaphroditism to dioecy in the genus Ophryotrocha.

Social conditions experienced prior to sexual maturity influence reproduction later in life in many animals. In simulta- neous hermaphrodites, variation in mating group size influences reproductive investment. As the mating group size increases, re- productive resources devoted to the female function decrease in favor of the male function. Prior to sexual maturity, many her- maphrodites have a protandrous phase during which they produce sperm and can fertilize hermaphrodites' eggs. In the simulta- neously hermaphroditic polychaete worm Ophryotrocha diadema, the cost of male reproduction during adolescence is spread over the whole energy budget of worms as shown by a reduced growth rate, a delayed age at sexual maturity and the shortening of life span compared to protandrous males that do not reproduce. Little is known on whether social conditions experienced dur- ing development affect reproductive investment of immature individuals. We investigated whether social conditions affected the length of the protandrous phase, body size and also the subsequent female fecundity of same-age protandrous individuals of O. diadema, which did not had to face competition for egg fertilization. Results show that in large group sizes protandrous males lengthened their protandrous phase, slowed down body growth and decreased their individual investment at the first egg laying compared to protandrous males that were reared in isolation. In the successive egg layings worms adjusted their egg output to the current social conditions. We interpreted these results as an indication that early social conditions represent a social stress result- ing in a reduction of the overall reproductive resources up to the first egg laying (Current Zoology 61 (6): 983-990, 2015). Keywords Social stress, Early experience, Ophryotrocha diadema, Female fecundity, Social environment

Foundresses of the social wasp Polistes biglumis were tested to see whether they were able to recognize alien eggs experimentally introduced into their own nests. Foundresses removed alien conspecific reproductive-destined eggs while they accepted worker-destined eggs. The results indicate that social wasps discriminate among eggs and that they discriminate against alien eggs destined to produce unrelated reproductives. P. biglumis is a strictly solitary founding species, with no reproductive competition within colonies; thus, brood discrimination abilities could have evolved as a counteradaptation against intra- and inter-specific brood parasitism.

In Polistes, nestmate recognition relies on the learning of recognition cues from the nest. When wasps recognize nestmates, they match the template learned with the odor of the encountered wasp. The social wasp Polistes biglumis use the homogeneous odor of their colony to recognize nestmates. When these colonies become host colonies of the social parasite P. atrimandibularis, colony odor is no longer homogeneous, as the parasite offspring have an odor that differs from that of their hosts. In trying to understand how the mechanism of nestmate recognition works in parasitized colonies and why parasite offspring are accepted by hosts, we tested the responses of resident Polistes biglumis wasps from parasitized and unparasitized colonies to newly emerged parasites and to nestmate and non-nestmate conspecifics. The experiments indicate that immediately upon eclosion both young parasites and young hosts lack a colony odor and that colony odor can be soon acquired from the accepting colony. In addition, while residents of nonparasitized colonies recognize only the odor of their species, resident hosts of parasitized colonies have learned a template that fits the odors of two species.

Mating opportunities fluctuate in the wild and hermaphrodites have the chance of partitioning reproductive resources between their two sexual functions accordingly, i.e., they have a plastic sex allocation. Plasticity is usually promoted by environmental fluctuations but may be affected by species-specific factors, which may be revealed by comparisons between related species. We tested whether polychaete worms of three related species of simultaneous hermaphrodites, Ophryotrocha diadema, Ophryotrocha adherens and Ophryotrocha gracilis, had plastic male and female allocation. We measured the costs of the female function and investigated whether the costs might affect the magnitude of plasticity in this function. To these aims, we exposed adult worms to three levels of mating opportunities and measured their female and male functions. In our experimental conditions, there was no adjustment in the male function, the cheapest function, whereas the three species differed in how they adjusted their allocation into the female function to mating opportunities. O. diadema and O. adherens worms exhibited highly plastic female allocation, and plasticity was consistent across three measures of female function. In contrast, O. gracilis worms had a fixed female allocation, irrespective of mating opportunities. Additionally, when the sexual functions were relatively costly, their plasticity was greater than when they were relatively cheap. However, the magnitude of the plasticity did not depend solely on species-specific costs of the function, but also on the features of the mating system of each species.

Parasite-induced alterations in host behaviour have been reported in a large number of taxa. However, some parasites are better than others to exploit the resources offered by their hosts. To date, our understanding of the extent to which some obligate parasites exploit social insect colonies is still limited. In this study, we examined parasite-mediated behavioural alterations of Polistes biglumis wasps parasitized by the obligate social parasite Polistes atrimandibularis by comparing host female-activity in parasitized and non-parasitized colonies. Host foundresses foraged more and rested less in parasitized than in non-parasitized colonies (controlling for the number of larvae in the nest, the time of day, and the day in the season). Next, we used short-term parasite removal experiments to investigate how social parasites manipulate their hosts. We found that parasitized hosts foraged more and rested less when social parasites were on the nest rather than after their removal, and we tested which kind of interactions occurred between parasites and hosts. P. atrimandibularis parasites may use mainly non-aggressive interactions (such as antennation and trophallaxis) to manipulate host activities, rather than visual, acoustic or chemical signals as other parasites do.

Ophryotrocha diadema is an outcrossing, simultaneous hermaphroditic polychaete with external fertilization. In isolated pairs, mature worms take turn contributing eggs upon the condition that their partners reciprocate egg donation. In dense populations, these worms do not reciprocate. Instead, they strongly compete for mating in their preferred male role and produce few eggs. This plastic sex allocation may result in an overall different reproductive performance: mean individual reproductive output will be larger in sparse than in dense populations. We tested this hypothesis by measuring the individual reproductive output (paternal and maternal offspring) of worms in sparse and dense replicated populations. In dense populations, mean individual reproductive output was fourfold lower than that in sparse populations. We hypothesise that such dramatic demographic costs are potentially widespread in outcrossing simultaneous hermaphrodites with external fertilization and plastic sex allocation. The re...

During the late pre-emergence phase, a foundress of the paper waspPolistes biglumis bimaculatus may be expelled by a conspecific female from her own nest (usurpation) or, less frequently, joined by another female of the same species (late association). The behaviour of femalePolistes biglumis bimaculatus, when usurping a conspecific colony or joining another foundress, is compared with that of foundresses on non-usurped colonies. The most conspicous difference is the intense abdomen stroking behaviour the usurper performs over the comb surface on the first days after usurpation. As observed in otherPolistes species, once usurpers and joiners arrive on a strange nest they will destroy most of the immature brood of the previous nest owner. Although host workers are not aggressive towards the intruder females, reproductive success of usurpers and joiners is low compared with that of legitimate foundresses. The same behaviours observed on usurped colonies are found in the obligate social parasites ofPolistes. These behaviours are therefore discussed in the context of the evolution of intra- and inter-specific parasitism.