On the further integration of cooperative breeding and cooperation theory

We present a synopsis about the commentaries to the target article "Integrating cooperative breeding into theoretical concepts of cooperation", in which we attempted to integrate general mechanisms to explain cooperative behaviour among unrelated individuals with classic concepts to explain helping behaviour in cooperative breeders that do not invoke kin-based benefits. Here we (1) summarize the positions of the commentators concerning the main issues we raised in the target article and discuss important criticisms and extensions. (2) We relate our target article to some recent reviews on the evolution of cooperation and, (3) clarify how we use terminology with regard to cooperation and cooperative behaviour. (4) We discuss several aspects that were raised with respect to cooperative interactions including by-product mutualism, generalised reciprocity and multi-level selection and, (5) examine the alternatives to our classification scheme as proposed by some commentaries. (6) Finally, we highlight several aspects that might hinder the application of game theoretical mechanisms of cooperation in cooperatively breeding systems. Although there is broad agreement that cooperative breeding theory should be integrated within the more general concepts of cooperation, there is some debate about how this may be achieved. We conclude that the contributions in this special issue provide a fruitful first step and ample suggestions for future directions with regard to a more unified framework of cooperation in cooperative breeders.     

Ecological and life-history correlates of cooperative breeding in South African birds

Our analyses of the incidence of cooperative breeding among South African birds differ from previous studies performed elsewhere in two respects. First, we distinguish between obligate (i.e. regular) and facultative (i.e. opportunistic) cooperative breeding species (OCS and FCS). Second, we have restricted our analyses to 217 South African bird species considered to be sufficiently well-studied in terms of their basic biology and life-history characteristics. This was done in order to control for the well-known bias against the often poorly-studied avifaunas of extreme environments such as rainforests and deserts. The results of our analysis do not accord fully with those of Australian birds by Ford et al. (1988). Cooperative breeding in South Africa is associated with seasonal environments, whereas in Australia the opposite is the case. Analyses of ecological factors that promote cooperative breeding among South African birds suggest that the evolutionary pathway to obligate and facultative breeding may be fundamentally different. First, OCS live mainly in savanna habitats that have predictable seasonal peaks in food availability, yet where the baseline level of food availability during the nonbreeding season is sufficient to support permanent residence by groups. Small to medium-sized birds of the African savannas are particularly vulnerable to avian predators, and foraging and roosting in permanent groups may enhance their survival. We propose that the benefits of obligate cooperative breeding are derived chiefly from survival of individuals away from the nest (i.e. during the nonbreeding season). Secondly, FCS live largely in unpredictable, seasonal steppe habitats. Under these conditions it may be impossible for birds to maintain permanent group territories, and variation in the tendency to breed cooperatively may depend largely on the opportunistic assessment of environmental conditions. We therefore suggest that birds (i.e. FCS) will opt to breed cooperatively only when conditions are unfavourable for independent breeding, and that the benefits thus accrued are chiefly related to reproduction.     

Experimentally induced helper dispersal in colonially breeding cooperative cichlids

The ‘benefits of philopatry’ hypothesis states that helpers in cooperatively breeding species derive higher benefits from remaining home, instead of dispersing and attempting to breed independently. We tested experimentally whether dispersal options influence dispersal propensity in the cooperatively breeding Lake Tanganyika cichlids Neolamprologus pulcher and N. savoryi. Cooperative groups of these fishes breed in densely packed colonies, surrounded by unoccupied, but apparently suitable breeding habitat. Breeding inside colonies and living in groups seems to benefit individuals, for example by early detection and deterrence of predators. We show that despite a slight preference of both species for habitat with a higher stone cover, 40% of the preferred habitat remained unoccupied. On average, the colonies contained a higher number of (1) predators of adults, juveniles and eggs, (2) shelter competitors, and (3) other species including potential food competitors, compared to the outside colony habitat. Apparently, habitat differences cannot explain why these cichlids breed in colonies. Accordingly, dispersal may not be limited by a lack of suitable breeding shelters, but by the relatively higher risk of establishing an outside- compared to a within-colony breeding territory. To test whether cichlids prefer within- to outside-colony breeding territories, we provided breeding shelters inside the colony and at the colony edge and studied helper dispersal. As expected, significantly more shelters were occupied within the colony compared to the edge. New breeding pairs with several helpers occupied these shelters. We conclude that although breeding habitat is plentiful outside the colonies, helpers delay dispersal to obtain a higher quality breeding position within the group or colony eventually, or they disperse in groups. Our results suggest that (1) group augmentation and Allee effects are generally important for dispersal decisions in cooperatively breeding cichlids, consistent with the ‘benefits of philopatry hypothesis’, and (2) habitat saturation cannot fully explain delayed dispersal in these species.     

Integrating genomic selection into dairy cattle breeding programmes: a review

Extensive genetic progress has been achieved in dairy cattle populations on many traits of economic importance because of efficient breeding programmes. Success of these programmes has relied on progeny testing of the best young males to accurately assess their genetic merit and hence their potential for breeding. Over the last few years, the integration of dense genomic information into statistical tools used to make selection decisions, commonly referred to as genomic selection, has enabled gains in predicting accuracy of breeding values for young animals without own performance. The possibility to select animals at an early stage allows defining new breeding strategies aimed at boosting genetic progress while reducing costs. The first objective of this article was to review methods used to model and optimize breeding schemes integrating genomic selection and to discuss their relative advantages and limitations. The second objective was to summarize the main results and perspectives on the use of genomic selection in practical breeding schemes, on the basis of the example of dairy cattle populations. Two main designs of breeding programmes integrating genomic selection were studied in dairy cattle. Genomic selection can be used either for pre-selecting males to be progeny tested or for selecting males to be used as active sires in the population. The first option produces moderate genetic gains without changing the structure of breeding programmes. The second option leads to large genetic gains, up to double those of conventional schemes because of a major reduction in the mean generation interval, but it requires greater changes in breeding programme structure. The literature suggests that genomic selection becomes more attractive when it is coupled with embryo transfer technologies to further increase selection intensity on the dam-to-sire pathway. The use of genomic information also offers new opportunities to improve preservation of genetic variation. However, recent simulation studies have shown that putting constraints on genomic inbreeding rates for defining optimal contributions of breeding animals could significantly reduce achievable genetic gain. Finally, the article summarizes the potential of genomic selection to include new traits in the breeding goal to meet societal demands regarding animal health and environmental efficiency in animal production.     

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.     

The evolution of cooperative breeding in the African cichlid fish,Neolamprologus pulcher

The conundrum of why subordinate individuals assist dominants at the expense of their own direct reproduction has received much theoretical and empirical attention over the last 50 years. During this time, birds and mammals have taken centre stage as model vertebrate systems for exploring why helpers help. However, fish have great potential for enhancing our understanding of the generality and adaptiveness of helping behaviour because of the ease with which they can be experimentally manipulated under controlled laboratory and field conditions. In particular, the freshwater African cichlid, Neolamprologus pulcher, has emerged as a promising model species for investigating the evolution of cooperative breeding, with 64 papers published on this species over the past 27 years. Here we clarify current knowledge pertaining to the costs and benefits of helping in N. pulcher by critically assessing the existing empirical evidence. We then provide a comprehensive examination of the evidence pertaining to four key hypotheses for why helpers might help: (1) kin selection; (2) pay‐to‐stay; (3) signals of prestige; and (4) group augmentation. For each hypothesis, we outline the underlying theory, address the appropriateness of N. pulcher as a model species and describe the key predictions and associated empirical tests. For N. pulcher, we demonstrate that the kin selection and group augmentation hypotheses have received partial support. One of the key predictions of the pay‐to‐stay hypothesis has failed to receive any support despite numerous laboratory and field studies; thus as it stands, the evidence for this hypothesis is weak. There have been no empirical investigations addressing the key predictions of the signals of prestige hypothesis. By outlining the key predictions of the various hypotheses, and highlighting how many of these remain to be tested explicitly, our review can be regarded as a roadmap in which potential paths for future empirical research into the evolution of cooperative breeding are proposed. Overall, we clarify what is currently known about cooperative breeding in N. pulcher, address discrepancies among studies, caution against incorrect inferences that have been drawn over the years and suggest promising avenues for future research in fishes and other taxonomic groups.     

Lateralization in response to social stimuli in a cooperatively breeding cichlid fish

Cerebral lateralization, an evolutionarily ancient and widespread phenomenon among vertebrates, is thought to bestow cognitive advantages. The advantages of lateralization at the individual-level do not necessarily require that the entire population share the same pattern of lateralization. In fact, directional bias in lateralization may lead to behavioural predictability and enhanced predator success or prey evasion. Recent theory has suggested that population-level lateralization may be favored if individuals are better able to perform coordinated behaviours, providing a distinct advantage in cooperative contexts. Here we test whether the highly social, cooperatively breeding cichlid fish Neolamprologus pulcher shows lateralized responses to a social stimulus. We found population-level biases in males; on average male N. pulcher use their right eye/left hemisphere to view their mirror image. Individual females had a preferred hemisphere, but these preferences appeared not to be directionally aligned among females. We discuss these results in the context of coordinated social behaviour and suggest future research directions.     

Mutation breeding of grain legumes

Summary Grain legumes are an important group of crop plants. They provide an essential source of protein food for many developing countries, but their production has gone down in favour of more profitable crops like cereals. Therefore, genetic improvement of grain legumes is urgently needed. The primary aim of grain legume breeding must be the increase of production through adaptation to more advanced cropping schemes and reduction of crop losses. Symbiotic nitrogen fixation as developed by natural evolution does not always seem to be compatible with the needed substantial increase in yield: It is not supplying sufficient nitrogen and supplementation by fertilizer is rather uneconomic. By genetic manipulation of the plant's regulatory system nitrogen fixation may become more effective and tolerant to high soil nitrogen levels. Through a number of mutation breeding projects in different countries involving all important grain legume species it has been proven that mutation induction is a good tool for supplementing the genetic variation available from natural evolution and from selection by man. High-yielding cultivars have been developed from induced mutants, which eventually also possess a more efficient nitrogen fixation capacity.     

Dynamic-persistence of cooperation in public good games when group size is dynamic

The evolution of cooperation is possible with a simple model of a population of agents that can move between groups. The agents play public good games within their group. The relative fitness of individuals within the whole population affects their number of offspring. Groups of cooperators evolve but over time are invaded by defectors which eventually results in the group's extinction. However, for small levels of migration and mutation, high levels of cooperation evolve at the population level. Thus, evolution of cooperation based on individual fitness without kin selection, indirect or direct reciprocity is possible. We provide an analysis of the parameters that affect cooperation, and describe the dynamics and distribution of population sizes over time.     

Environmental stability and the evolution of cooperative breeding in hornbills

Reproductive cooperation in social animals has been the focus of intensive research, yet the role of environmental factors in promoting such cooperation remains uncertain. A recent global analysis suggested that cooperative breeding in birds is a ‘bet-hedging’ strategy associated with climatic uncertainty, but it is unclear whether this mechanism applies generally or is restricted to the insectivorous passerines that predominate as cooperative breeders at the global scale. Here, we use a phylogenetic framework to assess the effect of climate on the evolution of cooperation in hornbills (Bucerotidae), an avian family characterized by frugivory and carnivory. We show that, in contrast to the global pattern, cooperative reproduction is positively associated with both inter- and intra-annual climatic stability. This reversed relationship implies that hornbills are relatively insensitive to climatic fluctuations, perhaps because of their dietary niche or increased body mass, both of which may remove the need for bet-hedging. We conclude that the relationship between climatic variability and cooperative breeding is inconsistent across taxa, and potentially mediated by life-history variation. These findings help to explain the mixed results of previous studies and highlight the likely shortcomings of global datasets inherently biased towards particular categories.     

Life histories and the evolution of cooperative breeding in mammals

While the evolution of cooperative breeding systems (where non-breeding helpers participate in rearing young produced by dominant females) has been restricted to lineages with socially monogamous mating systems where coefficients of relatedness between group members are usually high, not all monogamous lineages have produced species with cooperative breeding systems, suggesting that other factors constrain the evolution of cooperative breeding. Previous studies have suggested that life-history parameters, including longevity, may constrain the evolution of cooperative breeding. Here, we show that transitions to cooperative breeding across the mammalian phylogeny have been restricted to lineages where females produce multiple offspring per birth. We find no support for effects of longevity or of other life-history parameters. We suggest that the evolution of cooperative breeding has been restricted to monogamous lineages where helpers have the potential to increase the reproductive output of breeders.     

Multilevel selection: the evolution of cooperation in non-kin groups

Hamiltons (1964a, 1964b) landmark papers are rightly recognized as the formal basis for our understanding of the evolution of altruistic traits. However, Hamiltons equation as he originally expressed it is simplistic. A genetically oriented approach to studying multilevel selection can provide insights into how the terminology and assumptions used by Hamilton can be generalized. Using contextual analysis I demonstrated that Hamiltons rule actually embodies three distinct processes, group selection, individual selection, and transmission genetics or heritability. Whether an altruistic trait will evolve depends the balance of all of these factors. The genetical approach, and particularly, contextual analysis provides a means of separating these factors and examining them one at a time. Perhaps the greatest issue with Hamiltons equation is the interpretation of r. Hamilton (1964a) interpreted this as relatedness. In this paper I show that what Hamilton called relatedness is more generally interpreted as the proportion for variance among groups, and that many processes in addition to relatedness can increase the variance among groups. I also show that the evolution of an altruistic trait is driven by the ratio of the heritability at the group level to the heritability at the individual level. Under some circumstances this ratio can be greater than 1. In this situation altruism can evolve even if selection favoring selfish behavior is stronger than selection favoring altruism.     

Evolution of contingent altruism when cooperation is expensive

The ubiquity of cooperation has motivated a major research program over the last 50 years to discover ever more minimal conditions for the evolution of altruism. One important line of work is based on favoritism toward those who appear to be close relatives. Another important line is based on continuing interactions, whether between individuals (e.g., reciprocity) or between lines of descent in a viscous population. Here, we use an agent-based model to demonstrate a new mechanism that combines both lines of work to show when and how favoritism toward apparently similar others can evolve in the first place. The mechanism is the joint operation of viscosity and of tags (heritable, observable, and initially arbitrary characteristics), which serve as weak and potentially deceptive indicators of relatedness. Although tags are insufficient to support cooperation alone, we show that this joint mechanism vastly increases the range of environments in which contingent altruism can evolve in viscous populations. Even though our model is quite simple, the subtle dynamics underlying our results are not tractable using formal analytic tools (such as analysis of evolutionarily stable strategies), but are amenable to agent-based simulation.     

A case of cooperative breeding in the European Starling,Sturnus vulgaris

Cooperative breeding, where individuals other than the parents help to raise offspring, occurs in only ~9% of bird species. Although many starlings (Sturnidae) are cooperative breeders, the European starling (Sturnus vulgaris) has rarely been observed exhibiting this behavior. Only two other records exist, one of which was limited to a juvenile giving food to chicks that had already been collected by a parent (and hence providing limited help). Herein, we report a case of cooperative breeding by a juvenile European starling, which represents the second with any evidence of the juvenile collecting food independently and the first to document the extent of such help in the form of feeding rates. Over a period of at least 3 days, a juvenile starling assisted two parents to feed their second brood of the year, and it fed the chicks at the same rate as the adults (~3.5 feeds per hour). In considering potential explanations for this behavior, we conducted an ancestral state estimation of cooperative breeding across starlings and were able to eliminate the possibility that this is a rarely expressed behavior inherited from cooperatively breeding ancestors. Instead, we propose that our observations point to a behavioral innovation, which may be in response to environmental change such as climate change (which has previously been associated with cooperative breeding). Researchers working on birds should be alert to such behavior to determine whether this apparently new breeding strategy will increase as a potential adaptation to environmental change.     

The association between the emergence of cooperative breeding and clutch size

Previous theoretical work has suggested that smaller brood sizes helped facilitate the emergence of cooperative breeding in birds. However, recent empirical evidence has found no statistically significant difference between the clutch sizes of cooperative breeders and that of noncooperative breeders. One explanation for this finding is that while small clutch sizes may predispose species to cooperative breeding, the emergence of cooperative breeding itself may influence the evolution of clutch size. Here, we develop a set of models using population dynamics to describe how the emergence of cooperative breeding influences clutch size. We find, in contrast to previous theoretical work, that the emergence of cooperative breeding does not necessarily decrease (and under certain conditions may actually increase) clutch size. In particular, clutch size may increase after the emergence of cooperative breeding if helpers – philopatric individuals that assist their breeding relatives – are able to substantially improve breeder fecundity at low costs to their own survival, and if the association between breeder and helper is brief. In many cases, clutch size increases following the emergence of cooperative breeding not because it is optimal for the breeder, but as the result of breeder–helper conflict over resource allocation.     

Direct benefits and the evolution of female-biased cooperative breeding in Seychelles warblers

Abstract.— Inclusive fitness benefits have been suggested to be a major selective force behind the evolution of cooperative breeding. We investigated the fitness benefits selecting for cooperative breeding in the Seychelles warbler, Acrocephalus sechellensis . A microsatellite-based genotyping method was used to determine the relatedness of subordinates to group offspring in an isolated population of Seychelles warblers. The indirect and direct breeding benefits accruing to individual subordinates were then calculated for every successful breeding event over a three-year period. We show that female subordinates frequently gained parentage and that this, combined with high levels of extra group paternity, resulted in low levels of relatedness between subordinates and non descendent offspring within a territory. Direct breeding benefits were found to be significantly higher than indirect kin benefits for both female and male subordinates. As predicted, female subordinates gained significantly more direct breeding opportunities and therefore higher inclusive fitness benefits by being a subordinate within a group than did males. This may explain why most subordinates in the Seychelles warbler are female.     

Observations on the breeding behaviour of the Stripe‐breasted tit (Parus fasciiventer) in Bwindi Impenetrable National Park,Uganda

The motivation of this study was to investigate some hitherto unknown information on the breeding ecology of the Stripe‐breasted Tit (Parus fasciiventer) in Bwindi Impenetrable National Park, south‐western Uganda. Parus fasciiventer is one of the least studied and endemic bird species restricted to the montane forests of the Albertine Rift. Regionally, it is classified as near‐threatened. The study was carried out around the Institute of Tropical Forest Conservation Ruhija camp and the period of study was from January to June 2003. Data were generated through direct observation at the nest box sites of three active nests. Each of the nest boxes was monitored from the time of nest building to the time the chicks fledged. Results and comparative assessments from this study demonstrate that P. fasciiventer, compared with its temperate congeners like Great Tits (Parus major), Marsh Tits (Parus palustris), Crested Tits (Parus cristatus), Coal Tits (Parus ater) and Blue Tits (Parus caeruleus), raised small broods and had longer nestling period. The findings further revealed that the species is capable of raising more than one brood in a single breeding season and provide further evidence that it is a cooperative breeder. Parents participated equally in raising the young, an indication of pure parenting in the species.     

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.