Reproductive Partitioning Research Articles

Asymmetry in age suppresses reproduction in female woodland voles, Microtus pinetorum

The partitioning of reproduction in animal societies is a topic of interest to those studying animal behaviour. Under some conditions, two or more females may breed, but lack of reproduction by the younger females occurs frequently. Lack of reproduction by young females may be due to kin asymmetry, dominance asymmetry, or incest avoidance. We conducted breeding experiments to distinguish among these three hypotheses. We show that female reproduction within woodland vole family groups becomes skewed as the asymmetry in age, which is correlated with dominance, between females increases. When daughters were housed with their mothers and a potential mate and the age difference between females was large, we found a high level of skew as compared to females housed with same-age sisters and a potential mate or females housed only with a potential mate. We argue that dominance asymmetry is the best explanation for reproductive skew seen in female woodland voles that have access to unfamiliar, unrelated mates based on reproductive and previous behavioural observations.

Cichlids do not adjust reproductive skew to the availability of independent breeding options

Helpers in cooperatively breeding species forego all or part of their reproduction when remaining at home and assisting breeders to raise offspring. Different models of reproductive skew generate alternative predictions about the share of reproduction unrelated subordinates will get depending on the degree of ecological constraints. Concession models predict a larger share when independent breeding options are good, whereas restraint and tug-of-war models predict no effects on reproductive skew. We tested these predictions by determining the share of reproduction by unrelated male and female helpers in the Lake Tanganyika cichlid Neolamprologus pulcher depending on experimentally manipulated possibilities for helper dispersal and independent breeding and depending on helper size and sex. We created 32 breeding groups in the laboratory, consisting of two breeders and two helpers each, where only the helpers had access to a nearby dispersal compartment with (treatment) or without (control) breeding substrate, using a repeated measures design. We determined the paternity and maternity of 1185 offspring from 47 broods using five to nine DNA microsatellite loci and found that: (1) helpers participated in reproduction equally across the treatments, (2) large male helpers were significantly more likely to reproduce than small helpers, and (3) male helpers engaged in significantly more reproduction than female helpers. Interestingly, in four broods, extragroup helper males had fertilized part of the brood. No helper evictions from the group after helper reproduction were observed. Our results suggest that tug-of-war models based on competition over reproduction within groups describe best the reproductive skew observed in our study system. Female breeders produced larger clutches in the treatment compared to the control situation when the large helpers were males. This suggests that male breeder-male helper reproductive conflicts may be alleviated by females producing larger clutches with helpers around. Key words: Cichlidae, clutch size adjustment, cooperative breeding, ecological constraints, reproductive partitioning. [Behav Ecol]

Taming of the skew: transactional models fail to predict reproductive partitioning in the paper wasp Polistes dominulus

Female Polistes paper wasps can initiate colonies either solitarily or in cooperative groups. Reproduction is often distributed unequally in groups, even to the point of complete monopolization of breeding by the dominant group member. Transactional models of reproductive skew predict the degree of reproductive partitioning, assuming that the dominant controls group membership and will yield a proportion of reproduction to a subordinate as an incentive to stay peacefully in the group. Using a combination of demographic, genetic and morphological data from a population of P. dominulus, we test predictions of ‘classical’ two-person skew models as well as more complex ‘N-person’ models. This is the most comprehensive study of skew in this species to date, and the results generally do not support transactional models. We found no relationship between skew and relatedness for dyads, and complete skew was observed in unrelated groups despite the prediction for this population that such groups should not occur. In contrast to N-person model predictions, group size tended to increase with relatedness. Although we did find the predicted positive correlation between group size and skew for groups of nonrelatives, this relationship was weak. The zone of conflict between the predicted minimum and maximum staying incentives often spans the entire possible range of reproductive skew, suggesting that a ‘tug-of-war’ scenario may be more appropriate than a transactional framework for understanding within-colony dynamics. Overall, our results demonstrate that transactional skew models have little predictive power and are therefore unlikely to yield further insight into Polistes wasp societies.

Individual Recognition in Ant Queens

Personal relationships are the cornerstone of vertebrate societies, but insect societies are either too large for individual recognition, or their members were assumed to lack the necessary cognitive abilities . This paradigm has been challenged by the recent discovery that paper wasps recognize each other's unique facial color patterns . Individual recognition is advantageous when dominance hierarchies control the partitioning of work and reproduction . Here, we show that unrelated founding queens of the ant Pachycondyla villosa use chemical cues to recognize each other individually. Aggression was significantly lower in pairs of queens that had previously interacted than in pairs with similar social history but no experience with one another. Moreover, subordinates discriminated familiar and unfamiliar dominants in choice experiments in which physical contact, but not odor perception, was prevented and in tests with anaesthetized queens. The cuticular chemical profiles of queens were neither associated with dominance nor fertility and, therefore, do not represent status badges , and nestmate queens did not share a common odor. Personal recognition facilitates the maintenance of stable dominance hierarchies in these small societies. This suggests that the ability to discriminate between individual traits is selected for when it incurs net benefits for the resolution of conflict.

Reproductive skew in the Australian allodapine bee Exoneura robusta

Uneven sharing of reproduction (reproductive skew) among members of a cooperative animal society is one of the key features associated with advanced sociality and task specialization. Allocation of reproduction varies greatly among taxa, and reproductive skew models are evolutionary models that aim at explaining this variation. We tested reproductive skew theory using the Australian social allodapine bee Exoneura robusta. Reproductive skew was negatively correlated with relatedness, as predicted by the so-called tug-of-war model and the restraint model. Both models assume that a dominant breeder in a society does not have full control over the allocation of reproduction among group members, in contrast to classical concession models. Overall, the tug-of-war model seems to account better for the evolution of reproductive sharing in E. robusta than the restraint model. However, neither model can be ruled out, and a tug-of-war as well as a restraint model mechanism could apply in parallel in newly founded and overwintered colonies, respectively. This raises the possibility that skew models are not mutually exclusive and points to a more dynamic view on reproductive partitioning among breeders of an animal society.

Multiple reproductive strategies in a tropical hover wasp

Reproductive skew theory has been an important component of efforts to design a unifying theory of social evolution, as it aims to explain patterns of reproductive partitioning in animal societies as a function of relatedness, group productivity, fighting ability and ecological constraints on independent reproduction. However, empirical tests of the theory have often provided ambiguous or non-conclusive results, assumptions behind alternative models have rarely been tested, and theoretical elaborations have shown the limitations of the reproductive skew approach. Here we analyse a relatively large sample of colonies of the Stenogastrine wasp Parischnogaster mellyi with a powerful set of DNA microsatellite markers. We show that various apparently stable forms of social organisation co-exist in a single population, and that sharing of reproduction between related and unrelated egg-laying females occurs in some of the nests. Present reproductive skew theory appears to be at best partly sufficient to account for the observed complexity of social organisation. The observed patterns of colony composition and reproductive sharing are weakly consistent with the hypothesis of reproductive transactions, while they can more parsimoniously be explained by the life-history characteristics of the species.

No evidence for adaptive suppression of joint laying by dominant female Seychelles warblers: an experimental study

AbstractSeveral theoretical frameworks exist for explaining variation in reproductive allocation between same-sex individuals living within social groups. To determine this adequately, we need to know which party is more able to manipulate reproduction of the other. Theoretical models often sidestep this problem by making the assumption that dominants either have complete or partial control of reproduction by subordinates. This study clearly indicates that in the cooperatively breeding Seychelles warbler (Acrocephalus sechellensis) this assumption is not met. Seychelles warblers occupy year-round territories of different quality (measured as amount of insect food available). Joint laying, in which the dominant and subordinate females lay eggs in the same nest, decreases the fitness of primary females on low-quality territories, but not on high-quality territories. This study found good experimental evidence that dominant females on low-quality territories have no modes to suppress or prevent subordinate females from joint laying: (i) The frequency of joint laying in multi-female groups is independent of territory quality; (ii) There is no aggression among females at the nest around the time of egg laying at either low- or high-quality territories; (iii) Dominant females do not remove the other female's egg or experimentally introduced eggs, before or after laying their own. (iv) Dominant females do not reject an experimentally introduced egg through nest desertion. Given the absence of reproductive control, increased attention to alternative models of reproductive partitioning in vertebrate societies is needed and a realistic model has to take into account interactions within the sexes.

Multilevel selection and social evolution of insect societies.

How sterile, altruistic worker castes have evolved in social insects and how they are maintained have long been central topics in evolutionary biology. With the advance of kin selection theory, insect societies, in particular those of haplodiploid bees, ants, and wasps, have become highly suitable model systems for investigating the details of social evolution and recently also how within-group conflicts are resolved. Because insect societies typically do not consist of clones, conflicts among nestmates arise, for example about the partitioning of reproduction and the allocation of resources towards male and female sexuals. Variation in relatedness among group members therefore appears to have a profound influence on the social structure of groups. However, insect societies appear to be remarkably robust against such variation: division of labor and task allocation are often organized in more or less the same way in societies with high as in those with very low nestmate relatedness. To explain the discrepancy between predictions from kin structure and empirical data, it was suggested that constraints-such as the lack of power or information-prevent individuals from pursuing their own selfish interests. Applying a multilevel selection approach shows that these constraints are in fact group-level adaptation preventing or resolving intracolonial conflict. The mechanisms of conflict resolution in insect societies are similar to those at other levels in the biological hierarchy (e.g., in the genome or multicellular organisms): alignment of interests, fair lottery, and social control. Insect societies can thus be regarded as a level of selection with novelties that provide benefits beyond the scope of a solitary life. Therefore, relatedness is less important for the maintenance of insect societies, although it played a fundamental role in their evolution.

Tug-of-war over reproduction in a social bee.

One of the main transitions in evolution is the shift from solitary organisms to societies with reproductive division of labour. Understanding social evolution requires us to determine how ecological, social and genetic factors jointly influence group stability and partitioning of reproduction between group members. Here we test the role of the three key factors predicted to influence social evolution by experimentally manipulating them in a social allodapine bee. We show that increased relatedness between nestmates results in more even reproduction among group members and a greater productivity per individual. By contrast, the degree of reproductive skew is not influenced by the opportunity for solitary breeding or by the potential benefits of cooperation. Relatedness also has a positive effect on group stability and overall productivity. These findings are in line with predictions of the tug-of-war models, in which the degree of reproductive division of labour is determined primarily by selfish competition between group members. The alternative view, where the degree of reproductive skew is the outcome of a social contract between potential breeders, was not supported by the data.

Absence of individual sterility in thelytokous colonies of the ant Cerapachys biroi Forel (Formicidae, Cerapachyinae)

The reproductive partitioning generates a persistent conflict within insects societies and a sustained theoretical and empirical attention is devoted to understand its resolution. In that context, thelytokous parthenogenesis by workers is an intriguing phenomenon where each individual is virtually reproducing. This reproductive strategy, scarce among Formicidae, was studied in C. biroi, an obligatory thelytokous cerapachyine ant. Particularly, we searched for a reproductive division of labour in colonies assumed to be clonal. The results revealed that no sterile caste was present in the colonies. However, reproduction was linked both to a temporal polyethism, in which older workers ceased to lay as they became foragers, and to a morphological polyethism, illustrated by two morphological types of individuals displaying different task allocations and ovary capacities. Evolutionary implication of this uncommon social structure, seemingly free of traditional conflict and characterised by a reproduction evenly distributed among nestmates, is discussed from comparisons to other ant species with extreme kin structure.

Reproductive partitioning in communally breeding guira cuckoos, Guira guira

Guira cuckoos, Guira guira, exhibit a rare polygynandrous reproductive system with groups containing several male and female breeders, allowing for important tests of reproductive skew models. Female reproductive strategies involve leaving the group, varying clutch size, egg ejection and infanticide, among others. Here we examined the predictions of reproductive skew models relative to reproductive partitioning among females in groups. We used yolk protein electrophoresis to identify individual females’ eggs in joint nests. We found that reproductive partitioning favors early-laying females, which lay and incubate more eggs than females that begin laying later. Because the female that lays first tends to switch between repeated nesting bouts, and females do not always contribute eggs to each bout, female reproductive success tends to equalize within groups over time. The pattern of reproductive partitioning differs from that described for anis, another crotophagine joint-nester. We calculated reproductive skew indices for groups in 2 years, for both laying and incubation, as well as an overall population value. These were compared to random skew generated by simulations. Varying degrees of skew were found for different groups, and also across sequential nesting bouts of the same groups. Overall, however, skew did not deviate from random within the population. Nests that reached incubation tended to have lower skew values during the laying phase than nests terminated due to ejection of all eggs followed by desertion. Groups had higher reproductive skew indices in their first nesting bout of the season, and these nests frequently failed. These results illustrate the importance of social organization in determining not only individual, but group success in reproduction, and highlight the flexibility of vertebrate social behavior.

Reproductive sharing among queens in the ant Formica fusca

Reproductive sharing among cobreeders, in which reproductive shares may vary from equal contribution (low reproductive skew) to reproductive dominance by one individual (high reproductive skew), is a fundamental feature of animal societies. Recent theoretical work, the reproductive skew models, has focused on factors affecting the degree to which reproduction is skewed within a society. We used the parameters provided by skew models as a guideline to study determinants of reproductive sharing in polygyne ants. As a model system we used two-queen laboratory colonies of the ant Formica fusca in which the reproductive shares of each queen was assessed from offspring by using allozymes and DNA microsatellites. We tested how the different variables included in reproductive skew models (queen-queen relatedness, potential fighting ability, productivity, and worker relatedness reflected by queen number in the colony of origin) affect reproductive sharing among queens. The results showed that the relatedness among queens explained 26% of the variation in reproductive skew. The size difference between queens (reflecting potential fighting ability), colony productivity, and worker relatedness did not have an effect on reproductive partitioning among cobreeders. To our knowledge, this is the first study to test for the effects of various determinants of skew in an experimental setting. Copyright 2003.

Costs and benefits of subordinate queens in colonies of the ant, Leptothorax gredleri.

Queens of some species of social insects form dominance hierarchies in which only the top-ranking individual reproduces. Such unequal partitioning of reproduction can be stable when subordinate queens increase their inclusive fitness indirectly by helping to rear a related dominant queen's offspring. We investigated whether subordinate queens of the ant, Leptothorax gredleri, affect the reproductive success of the dominant queen. In laboratory colonies with two queens, first eggs were laid approximately 20 days later than in colonies with a single queen, presumably due to aggressive competition among nestmate queens. Nevertheless, two-queen colonies produced on average more brood than one-queen colonies, although egg laying was completely or almost completely monopolized by one single queen. The presence of a subordinate queen therefore appears to increase the productivity of the dominant.

From individual control to majority rule: extending transactional models of reproductive skew in animal societies.

Transactional concession models of social evolution explain the reproductive skew within groups by assuming that a dominant individual completely controls the allocation of reproduction to other group members. The models predict when the dominant will benefit from donating parcels of reproduction to other members in return for peaceful cooperation. Using linear programming methods, we present a 'majority-rules' model in which the summed actions of all society members, each with equal power, completely determine the reproductive share of any single member. The majority-rules model predicts that, despite the diffusion of power, a 'virtual dominant' (a dominant lacking special behavioural power) will emerge and that the reproductive skew will be exactly that predicted if the virtual dominant were to control completely the group's reproductive partitioning. The virtual dominant is the individual to which group members have the maximum average genetic relatedness. This result greatly broadens the applicability of transactional models of reproductive skew to social groups of any size, such as large-colony eusocial insects, and explains why queens in such colonies can achieve reproductive domination without any behavioural enforcement. Moreover, the majority-rules model unifies transactional-skew theory with models of worker policing and even generates a new theory for the cooperation among somatic cells in a multicellular organism.

Female Control of the Distribution of Paternity in Cooperative Breeders

Models of reproductive skew have shed light on why animal societies vary in the partitioning of reproduction among group members. However, their application to cooperative vertebrate societies remains controversial. A particular problem is that previous models assume that skew in paternity is determined by interactions among males and males only. This conflicts with observations from many species that indicate that females exert control over the distribution of paternity. Here we address this shortfall in the current theory by developing two models to explore the expected patterns of skew in three member groups in which a female controls the allocation of paternity among two males. The first "staying incentive" model extends previous "transactional" (or "concession") models to examine the conditions where females will be willing to share reproduction among a dominant and a subordinate male to retain the subordinate in the group. The second "work incentive" model explores patterns of skew where females allocate paternity in order to maximize the amount of care their offspring receive. The models make contrasting predictions about the nature of male-female conflict over reproduction and also about the relationships between skew and relatedness, ecological constraints, the relative quality of the subordinate male, and the relative cost of care for the two males. These divergent predictions provide a schema by which the evolutionary causes of variation in skew among males can be evaluated.

Proximate Determinants of Reproductive Skew in Polygyne Colonies of the AntFormica fusca

AbstractUnderstanding 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 antFormica 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 theFormicaants, direct interactions as a means for gaining reproductive dominance have lost their importance.

Queen reproduction, chemical signalling and worker behaviour in polygyne colonies of the ant Formica fusca

Potential reproductive conflicts are common in social insects and may occur between and within castes. In multiqueen (polygyne) colonies of ants, reproductive conflicts among coexisting queens may be resolved by aggressive interactions and/or by pheromonal signalling. Pheromonal signals may be directed at workers, which may adjust the reproductive shares of queens behaviourally. Workers are expected to favour a queen that is more likely to be their mother and to produce offspring of close kin to them. We used microsatellite markers to study reproductive partitioning between cobreeding Formica fusca queens in a laboratory experiment where workers received a choice between two queens. We expected queens of this species to communicate their reproductive status by chemical communication, because no aggressive interactions between queens have been observed. We found that queens of different reproductive status (with majority, minority or no production) differed in their cuticular hydrocarbon (CHC) profiles. The fecundity of a queen was associated with worker behaviour; the higher a queen's fecundity, the more attention she received from workers. Our results suggest that a queen fecundity signal is encoded in her CHC profile and acts as a pheromone for workers, which respond to the signal by discriminating between queens. Copyright 2002 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour

Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew

Who reproduces in colonies of social insects is determined by some combination of direct competition and more peaceful convention. We studied these two alternatives in foundresses of the paper wasp, Polistes carolina, by examining two different contexts: what determines who becomes the dominant reproductive and what determines the amount of reproduction obtained by subordinates. The dominant queen on most nests was the foundress to arrive first, rather than the largest foundress, expected to be best at fighting. This suggests that dominance is initially determined by convention, although the persistence of some aggressive conflict throughout the foundress period suggests that this convention is not absolute. Attempts to explain the division of reproduction using several skew theories were generally unsuccessful. Skew was not correlated with relatedness, size differences, colony productivity, and challenges by the subordinate. P. carolina showed high constraints against solitary nesting, with a minority of females attempting to nest alone, and none succeeding. In this situation, most skew theories predict that group stability will be independent of relatedness, yet nearly all collected subordinates were full sisters to the queen. Reproductive partitioning in early P. carolina colonies may have more to do with enhancing worker production than with conflict over direct fitness. Key words: Hymenoptera, microsatellites, Polistes, Polistinae, queues, reproductive dominance, reproductive skew, wasps. [Behav Ecol 13:531–542 (2002)]

Reproductive skew in the polygynandrous acorn woodpecker.

Reproductive skew models, which focus on the degree to which reproduction is shared equally (low skew) or monopolized by a single individual (high skew) within groups, have been heralded as providing a general unifying framework for understanding the factors determining social evolution. Here, we test the ability of optimal skew, or "transactional," models, which predict the level of skew necessary to promote stable associations of dominants and subordinates, rather than independent breeding, to predict reproductive partitioning in the acorn woodpecker (Melanerpes formicivorus). This species provides a key test case because only a few vertebrates exhibit polygynandry (multiple breeders of both sexes within a group). Contrary to the predictions of the models, joint-nesting females share reproduction more equitably than expected, apparently because egg destruction and the inability of females to defend their eggs from cobreeders eliminate any possibility for one female to control reproduction. For males, however, reproductive skew is high, with the most successful male siring over three times as many young as the next most successful male. Although this result is consistent with optimal skew models, other aspects of male behavior are not; in particular, the reproductively most successful male frequently switches between nests produced by the same set of cobreeders, and we were unable to detect any phenotypic correlate of success. These results are consistent with an alternative null model in which cobreeder males have equal chance of paternity, but paternity of offspring within broods is nonindependent as a consequence of female, rather than male, control.

Intracolonial patterns of reproduction in the queen-size dimorphic ant Leptothorax rugatulus

Animals that live in genetically heterogeneous groups are faced with a combination of cooperation and conflict. Reproductive skew theory aims to provide a unified theory of the partitioning of reproduction in animal societies by combining genetic, demographic, and environmental factors. Although theoretical elaborations abound, empirical data are rare. Specifically, explicit intraspecific tests are scarce and have provided conflicting results. We present data on reproductive partitioning among queens in the ant Leptothorax rugatulus with special emphasis on relatedness and body size. Relatedness was negatively correlated to skew in sexual offspring and uncorrelated to skew in total offspring. Body size was not correlated to a queen's reproductive share. Thus, we did not find any support for the classic optimal skew models that are based on concessions. In artificial colonies, composed of randomly selected, unrelated workers and queens, reproductive skew was higher than in natural colonies, which suggested that unequal reproduction among queens could arise without nepotism by workers. Again, a queen's body size was not a good indicator of her reproductive share, but egg laying rate was. In colonies that contained large and small queens, small queens produced proportionally more sexual offspring. Although this result is in accordance with the kin conflict over caste determination hypothesis, it is more plausibly explained by an adaptation of the caste ratios to alternative dispersal tactics.