Promiscuity and the evolution of cooperative breeding

Empirical data suggest that low levels of promiscuity have played a key role in the evolution of cooperative breeding and eusociality. However, from a theoretical perspective, low levels of promiscuity can favour dispersal away from the natal patch, and have been argued to select against cooperation in a way that cannot be explained by inclusive fitness theory. Here, we use an inclusive fitness approach to model selection to stay and help in a simple patch-structured population, with strict density dependence, where helping increases the survival of the breeder on the patch. Our model predicts that the level of promiscuity has either no influence or a slightly positive influence on selection for helping. This prediction is driven by the fact that, in our model, staying to help leads to increased competition between relatives for the breeding position-when promiscuity is low (and relatedness is high), the best way to aid relatives is by dispersing to avoid competing with them. Furthermore, we found the same results with an individual-based simulation, showing that this is not an area where inclusive fitness theory 'gets it wrong'. We suggest that our predicted influence of promiscuity is sensitive to biological assumptions, and that if a possibly more biologically relevant scenario were examined, where helping provided fecundity benefits and there was not strict density dependence, then low levels of promiscuity would favour helping, as has been observed empirically.     

Multilocus heterozygosity, parental relatedness and individual fitness components in a wild mountain goat, Oreamnos americanus population

Matings between relatives lead to a decrease in offspring genetic diversity which can reduce fitness, a phenomenon known as inbreeding depression. Because alpine ungulates generally live in small structured populations and often exhibit a polygynous mating system, they are susceptible to inbreeding. Here, we used marker-based measures of pairwise genetic relatedness and inbreeding to investigate the fitness consequences of matings between relatives in a long-term study population of mountain goats ( Oreamnos americanus ) at Caw Ridge, Alberta, Canada. We first assessed whether individuals avoided mating with kin by comparing actual and random mating pairs according to their estimated genetic relatedness, which was derived from 25 unlinked polymorphic microsatellite markers and reflected pedigree relatedness. We then examined whether individual multilocus heterozygosity H , used as a measure of inbreeding, was predicted by parental relatedness and associated with yearling survival and the annual probability of giving birth to a kid in adult females. Breeding pairs identified by genetic parentage analyses of offspring that survived to 1 year of age were less genetically related than expected under random matings. Parental relatedness was negatively correlated with offspring H , and more heterozygous yearlings had higher survival to 2 years of age. The probability of giving birth was not affected by H in adult females. Because kids that survived to yearling age were mainly produced by less genetically related parents, our results suggest that some individuals experienced inbreeding depression in early life. Future research will be required to quantify the levels of gene flow between different herds, and evaluate their effects on population genetic diversity and dynamics.     

The effects of inbreeding, genetic dissimilarity and phenotype on male reproductive success in a dioecious plant

Pollen fate can strongly affect the genetic structure of populations with restricted gene flow and significant inbreeding risk. We established an experimental population of inbred and outbred Silene latifolia plants to evaluate the effects of (i) inbreeding depression, (ii) phenotypic variation and (iii) relatedness between mates on male fitness under natural pollination. Paternity analysis revealed that outbred males sired significantly more offspring than inbred males. Independently of the effects of inbreeding, male fitness depended on several male traits, including a sexually dimorphic (flower number) and a gametophytic trait (in vitro pollen germination rate). In addition, full-sib matings were less frequent than randomly expected. Thus, inbreeding, phenotype and genetic dissimilarity simultaneously affect male fitness in this animal-pollinated plant. While inbreeding depression might threaten population persistence, the deficiency of effective matings between sibs and the higher fitness of outbred males will reduce its occurrence and counter genetic erosion.     

Demography of male reproductive queues in cooperatively breeding superb fairy-wrens Malurus cyaneus

1. Subordinate helpers in cooperative societies may gain both immediate and future benefits, including paternity and territorial inheritance. However, if such opportunities correlate with rank in the queue, it is unclear why such queues should be stable. 2. In cooperatively breeding superb fairy-wrens Malurus cyaneus, only males are generally philopatric, and form stable hierarchical queues for the dominant position. 3. Male opportunities for reproduction are influenced both by their dominance status within the group, and their relatedness to the breeding female. For young queuing subordinates, the breeding female is typically their mother. Because of incest avoidance, reproduction is possible only through extra-group mating, even if the dominant position is achieved while the mother is still on the territory. If the mother dies while the helper is still a subordinate, he can seek matings both outside the group, and with the unrelated replacement female within the group. Finally, males can achieve the dominant position and pair with an unrelated female by inheritance, dispersal to a neighbouring vacancy, or by forming a liaison with an immigrant subordinate female that causes fission of the natal territory. 4. On average males spent more time living with unrelated females than with their mother. Subordinate males gained no survival advantages when living with their mother rather than an unrelated female, contrary to the prediction that parents facilitate the survival of their offspring. 5. Dominants and subordinates also had similar survival. Mortality accelerated over time, probably because older males invest more in extra-group courtship display. 6. Fairy-wren queues are likely to be stable because older birds are superior, and because extra-pair mating provides direct benefits to subordinates.     

Causes and consequences of incest avoidance in the cooperatively breeding mole-rat, Cryptomys darlingi (Bathyergidae)

A number of social mole-rat species maintain a strong reproductive skew (only one breeding pair in the group) solely through incest avoidance. Incest avoidance probably evolved for one of two reasons, namely for actually maintaining a reproductive skew or, alternatively, to avoid high inbreeding depression. In the latter case a strong reproductive skew would result as a fortuitous by-product of the combination of a cloistral family life style of mole-rats and incest avoidance. We undertook breeding experiments in which the fertility of pairs of unrelated individuals were compared with that of pairs of double first cousins. Inbreeding depression was remarkably high and an accompanying model suggests that it may be sufficient to support the idea that strong incest avoidance evolved primarily to eliminate the costs of inbreeding and subsequently facilitated the evolution of reproductive skew.     

Differential allocation in a lekking bird: females lay larger eggs and are more likely to have male chicks when they mate with less related males

The differential allocation hypothesis predicts increased investment in offspring when females mate with high-quality males. Few studies have tested whether investment varies with mate relatedness, despite evidence that non-additive gene action influences mate and offspring genetic quality. We tested whether female lekking lance-tailed manakins (Chiroxiphia lanceolata) adjust offspring sex and egg volume in response to mate attractiveness (annual reproductive success, ARS), heterozygosity and relatedness. Across 968 offspring, the probability of being male decreased with increasing parental relatedness but not father ARS or heterozygosity. This correlation tended to diminish with increasing lay-date. Across 162 offspring, egg volume correlated negatively with parental relatedness and varied with lay-date, but was unrelated to father ARS or heterozygosity. Offspring sex and egg size were unrelated to maternal age. Comparisons of maternal half-siblings in broods with no mortality produced similar results, indicating differential allocation rather than covariation between female quality and relatedness or sex-specific inbreeding depression in survival. As males suffer greater inbreeding depression, overproducing females after mating with related males may reduce fitness costs of inbreeding in a system with no inbreeding avoidance, while biasing the sex of outbred offspring towards males may maximize fitness via increased mating success of outbred sons.     

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta)

Measurement of reproductive skew in social groups is fundamentalto understanding the evolution and maintenance of sociality,as it determines the immediate fitness benefits to helpers ofstaying and helping in a group. However, there is a lack ofstudies in natural populations that provide reliable measuresof reproductive skew and the correlates of reproductive success,particularly in vertebrates. We present results of a study thatuses a combination of field and genetic (microsatellite) dataon a cooperatively breeding mongoose, the meerkat (Suricatasuricatta). We sampled 458 individuals from 16 groups at twosites and analyzed parentage of pups in 110 litters with upto 12 microsatellites. We show that there is strong reproductiveskew in favor of dominants, but that the extent of skew differsbetween the sexes and between different sites. Our data suggestthat the reproductive skew arises from incest avoidance andreproductive suppression of the subordinates by the dominants.     

Age-dependent inbreeding risk and offspring fitness costs in female black grouse

Dispersal is an important mechanism used to avoid inbreeding. However, dispersal may only be effective for part of an individual's lifespan since, post-dispersal individuals that breed over multiple reproductive events may risk mating with kin of the philopatric sex as they age. We tested this hypothesis in black grouse Tetrao tetrix, and show that yearling females never mated with close relatives whereas older females did. However, matings were not with direct kin suggesting that short-distance dispersal to sites containing kin and subsequent overlap of reproductive lifespans between males and females were causing this pattern. Chick mass was lower when kinship was high, suggesting important fitness costs associated with inbred matings. This study shows that increased inbreeding risk might be a widespread yet rarely considered cost of ageing.