The evolution of cooperative breeding in birds: kinship,dispersal and life history

The evolution of cooperation among animals has posed a major problem for evolutionary biologists, and despite decades of research into avian cooperative breeding systems, many questions about the evolution of their societies remain unresolved. A review of the kin structure of avian societies shows that a large majority live in kin-based groups. This is consistent with the proposed evolutionary routes to cooperative breeding via delayed dispersal leading to family formation, or limited dispersal leading to kin neighbourhoods. Hypotheses proposed to explain the evolution of cooperative breeding systems have focused on the role of population viscosity, induced by ecological/demographic constraints or benefits of philopatry, in generating this kin structure. However, comparative analyses have failed to generate robust predictions about the nature of those constraints, nor differentiated between the viscosity of social and non-social populations, except at a coarse level. I consider deficiencies in our understanding of how avian dispersal strategies differ between social and non-social species, and suggest that research has focused too narrowly on population viscosity and that a broader perspective that encompasses life history and demographic processes may provide fresh insights into the evolution of avian societies.     

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 joint evolution of mating system, floral traits and life history in Clarkia (Onagraceae): genetic constraints vs. independent evolution

Genetic correlations caused by pleiotropy or linkage disequilibrium may influence the joint evolution of multiple traits as populations or taxa diverge. The evolutionary transition from outcrossing to selfing has occurred numerous times and is often accompanied by phenotypic and genetic changes in multiple traits such as flower size, pollen-ovule ratio, stigma and anther maturity and the age of reproductive maturity. Determining whether the recurring patterns of multitrait change are because of selection on each trait independently and/or the result of genetic correlations among traits can shed light on the mechanism that accounts for such convergence. Here, we evaluate whether floral traits are genetically correlated with each other and/or with whole-plant traits within- and between-populations and taxa. We report results from a greenhouse study conducted on two pairs of sister taxa with contrasting mating systems: the autogamously selfing Clarkia exilis and its predominantly outcrossing progenitor C. unguiculata and the autogamous Clarkia xantiana ssp. parviflora and its outcrossing progenitor C. xantiana ssp. xantiana. We examined variation within and covariation among maternal families in three populations of each taxon with respect to the age at first flower, the rate of successive flower production and the number of days between bud break and anther dehiscence and stigma receptivity within individual flowers. Based on phenotypic divergence between sister taxa, bivariate regressions, correlations among maternal family means and analysis of covariance (ancova), we did not find unilateral support indicating that genetic constraints govern the joint distribution of floral and whole-plant traits.     

The Maturity Index,the evolution of nematode life history traits,adaptive radiation and cp-scaling

Nematodes are increasingly being used in environmental studies. One of the potential parameters to measure the impact of disturbances and to monitor changes in structure and functioning of the below-ground ecosystem is the nematode Maturity Index; an index based on the proportion of colonizers (r-strategists s.l.) and persisters (K-strategists s.l.) in samples. In this paper the original allocation of nematode taxa on the colonizer-persister scale, and the tolerance and sensitivity of colonizers and persisters are discussed from an evolutionary viewpoint. The phenomenon that neither relative egg size nor body length is an unequivocal character to scale nematodes suggests that the main selection for life history traits occurred independently in the major evolutionary branches. This revised version was published online in June 2006 with corrections to the Cover Date.     

Thermal evolution of pre-adult life history traits in Drosophila melanogaster

Replicated lines of Drosophila melanogaster were allowed to evolve in population cage culture at 16.5° C or 25° C for five years. Their larval and pupal development times, larval growth rates, larval critical weights for pupariation and pre-adult survival rates were then measured at both temperatures. Pre-adult survival showed evidence of adaptation of the lines to their thermal selection regimes, with each set of lines showing superior survival when tested at the temperature at which they had been evolving. Pupal periods were similar for all lines when growing at 16.5° C but, at 25° C, the low temperature lines had the longer pupal periods. Irrespective of experimental temperature, low temperature lines grew faster and had shorter larval development periods than the high temperature lines. Larval critical weights for pupariation were higher in the low temperature lines at the low experimental temperature, and higher in the high temperature lines at the higher experimental temperature. The correlations between these traits induced by thermal evolution were in general different from or opposite to the genetic correlations found within a single temperature.     

Towards a unified theory of cooperative breeding: the role of ecology and life history re-examined

We present quantitative models that unify several adaptive hypotheses for the evolution of cooperative breeding in a single framework: the ecological constraints hypothesis, the life-history hypothesis and the benefits-of-philopatry hypothesis. Our goal is to explain interspecific variation in the occurrence of cooperative breeding in terms of interspecific variation in life-history traits and ecological conditions. We analyse two models, according to whether or not helpers can inherit their parents' territory. Major results are (i) territory inheritance always promotes cooperative breeding; (ii) if territories are not inherited, neither ecological constraints nor variation in life-history traits predict interspecific variation in cooperative breeding; and (iii) if territories are inherited, the mechanism of density regulation is crucial in determining which factors promote cooperative breeding. If density dependence acts on the probability to obtain a free territory or on the survival of dispersers, variation in ecological constraints cannot explain variation in cooperative breeding. Lower adult mortality favours helping, not because it reduces the availability of free territories, but because it enhances the direct benefits of helpers. If density dependence acts on fecundity, lower probability of obtaining a free territory and lower survival of dispersers promote cooperative breeding. In this case, lower adult mortality works against the evolution of helping. We suggest that the difference between birds and social insects in the covariance between cooperative breeding and life-history traits is due to different mechanisms of density regulation that operate in these taxa, and we explain how natural selection on habitat choice might have caused these different mechanisms to operate.     

Ecological indicator values and life history traits of terricolous lichens of the Western Carpathians

Plant indicator values are widely used in ecological studies, but they are not well developed for cryptogams, what prevents their application in some environments such as lichen-rich habitats. The aim of this study was to determine the ecological indicator values of terricolous lichens occurring in the Western Carpathians. A total of 271 lichen taxa from the eastern part of Central Europe in Czech Republic, Slovakia, Hungary and Austria are listed and evaluated. Their known indicator values for light conditions, climate (temperature, continentality), substratum (humidity, soil reaction-pH, nutrients, eutrophication) were reviewed or modified, and original values were established for taxa with missing information. Besides the traditional ordinal scale, the index of variability was established to distinguish between generalists and specialists in particular applications. Our list further contains important species traits such as ecological strategies (growth and life forms, photobiont type, substrate, reproduction) and geographic values (geographical elements, threat, frequency) allowing applications in functional ecology and macroecology. Our database can be easily associated with widely used software for the analysis of vegetation data allowing the indication of ecological conditions in lichen-rich vegetation types in currently developed large-scale vegetation surveys.     

Life history constraints on the evolution of abbreviated life cycles in parasitic trematodes

Abbreviations of the complex life cycle of trematodes, from three to two hosts, have occurred repeatedly and independently among trematode lineages. This is usually facultative and achieved via progenesis: following encystment in the second intermediate host, the metacercaria develops precociously into an egg-producing adult, bypassing the need to reach a definitive host. Given that it provides relatively cheap insurance against a shortage of definitive hosts, it is not clear why facultative progenesis has only evolved in a few taxa. Here a comparative approach is used to test whether progenetic trematodes are characterized by larger body size and egg volumes, two traits that correlate with other key life history features, than other trematodes. These traits may constrain the evolution of progenesis, because precocious maturation might be impossible when the size difference between the metacercaria and a reproductive adult is too large. First, trematode species belonging to genera in which progenesis has been documented were found not to differ significantly from other trematode species. Second, using within-genus paired comparisons across 19 genera in which progenesis has been reported, progenetic species did not differ, with respect to body size or egg size, from their non-progenetic congeners. Third, using intraspecific paired comparisons in species where progenesis is facultative, no difference was observed in the sizes of eggs produced by worms in both the intermediate and definitive host, suggesting that opting for progenesis does not influence the size of a worm's eggs. Overall, the lack of obvious differences in body or egg size between trematodes with truncated life cycles and those with the normal three-host cycle indicates that basic life history characteristics are not acting as constraints on the evolution of progenesis; trematodes of all sizes can do it. Why facultative progenesis is not more widespread remains a mystery.     

Ecological adaptation drives wood frog population divergence in life history traits

Phenotypic variation among populations is thought to be generated from spatial heterogeneity in environments that exert selection pressures that overcome the effects of gene flow and genetic drift. Here, we tested for evidence of isolation by distance or by ecology (i.e., ecological adaptation) to generate variation in early life history traits and phenotypic plasticity among 13 wood frog populations spanning 1200 km and 7° latitude. We conducted a common garden experiment and related trait variation to an ecological gradient derived from an ecological niche model (ENM) validated to account for population density variation. Shorter larval periods, smaller body weight, and relative leg lengths were exhibited by populations with colder mean annual temperatures, greater precipitation, and less seasonality in precipitation and higher population density (high-suitability ENM values). After accounting for neutral genetic variation, the Q_ST–F_ST analysis supported ecological selection as the key process generating population divergence. Further, the relationship between ecology and traits was dependent upon larval density. Specifically, high-suitability/high-density populations in the northern part of the range were better at coping with greater conspecific competition, evidenced by greater postmetamorphic survival and no difference in body weight when reared under stressful conditions of high larval density. Our results support that both climate and competition selection pressures drive clinal variation in larval and metamorphic traits in this species. Range-wide studies like this one are essential for accurate predictions of population’s responses to ongoing ecological change.Subject terms: Biogeography, Ecological modelling, Evolutionary ecology, Evolution     

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.     

Correlated contemporary evolution of life history traits in New Zealand Chinook salmon, Oncorhynchus tshawytscha

Size at age and age at maturity are important life history traits, affecting individual fitness and population demography. In salmon and other organisms, size and growth rate are commonly considered cues for maturation and thus age at maturity may or may not evolve independently of these features. Recent concerns surrounding the potential phenotypic and demographic responses of populations facing anthropogenic disturbances, such as climate change and harvest, place a premium on understanding the evolutionary genetic basis for evolution in size at age and age at maturity. In this study, we present the findings from a set of common-garden rearing experiments that empirically assess the heritable basis of phenotypic divergence in size at age and age at maturity in Chinook salmon (Oncorhynchus tshawytscha) populations introduced to New Zealand. We found consistent evidence of heritable differences among populations in both size at age and age at maturity, often corresponding to patterns observed in the wild. Populations diverged in size and growth profiles, even when accounting for eventual age at maturation. By contrast, most, but not all, cases of divergence in age at maturity were driven by the differences in size or growth rate rather than differences in the threshold relationship linking growth rate and probability of maturation. These findings help us understand how life histories may evolve through trait interactions in populations exposed to natural and anthropogenic disturbances, and how we might best detect such evolution.     

The evolution of cooperative breeding through group augmentation

Some individuals (helpers) in cooperatively breeding species provide alloparental care and often suppress their own reproduction. Kin selection is clearly an important explanation for such behaviour, but a possible alternative is group augmentation where individuals survive or reproduce better in large groups and where it therefore pays to recruit new members to the group. The evolutionary stability of group augmentation is currently disputed. We model evolutionarily stable helping strategies by following the dynamics of social groups with varying degrees of subordinate help. We also distinguish between passive augmentation, where a group member benefits from the mere presence of others, and active augmentation, where their presence as such is neutral or harmful, but where helping to recruit new group members may still be beneficial if they in turn actively provide help for the current reproductives ('delayed reciprocity'). The results show that group augmentation (either passive or active) can be evolutionarily stable and explain costly helping by non-reproductive subordinates, either alone or leading to elevated help levels when acting in concert with kin selection. Group augmentation can thus potentially explain the weak relationships between relatedness and helping behaviour that are observed in some cooperatively breeding species. In some cases, the superior mutualistic performance of cooperatively behaving groups can generate an incentive to stay and help which is strong enough to make ecological constraints unnecessary for explaining the stability of cooperatively breeding groups.     

Thermal evolution of pre-adult life history traits, geometric size and shape, and developmental stability in Drosophila subobscura

Replicated lines of Drosophila subobscura originating from a large outbred stock collected at the estimated Chilean epicentre (Puerto Montt) of the original New World invasion were allowed to evolve under controlled conditions of larval crowding for 3.5 years at three temperature levels (13, 18 and 22 degrees C). Several pre-adult life history traits (development time, survival and competitive ability), adult life history related traits (wing size, wing shape and wing-aspect ratio), and wing size and shape asymmetries were measured at the three temperatures. Cold-adapted (13 degrees C) populations evolved longer development times and showed lower survival at the highest developmental temperature. No divergence for wing size was detected following adaptation to temperature extremes (13 and 22 degrees C), in agreement with earlier observations, but wing shape changes were obvious as a result of both thermal adaptation and development at different temperatures. However, the evolutionary trends observed for the wing-aspect ratio were inconsistent with an adaptive hypothesis. There was some indication that wing shape asymmetry has evolutionarily increased in warm-adapted populations, which suggests that there is additive genetic variation for fluctuating asymmetry and that it can evolve under rapid environmental changes caused by thermal stress. Overall, our results cast strong doubts on the hypothesis that body size itself is the target of selection, and suggest that pre-adult life history traits are more closely related to thermal adaptation.     

Sex,long life and the evolutionary transition to cooperative breeding in birds

Long life is a typical feature of individuals living in cooperative societies. One explanation is that group living lowers mortality, which selects for longer life. Alternatively, long life may make the evolution of cooperation more likely by ensuring a long breeding tenure, making helping behaviour and queuing for breeding positions worthwhile. The benefit of queuing will, however, depend on whether individuals gain indirect fitness benefits while helping, which is determined by female promiscuity. Where promiscuity is high and therefore the indirect fitness benefits of helping are low, cooperation can still be favoured by an even longer life span. We present the results of comparative analyses designed to test the likelihood of a causal relationship between longevity and cooperative breeding by reconstructing ancestral states of cooperative breeding across birds, and by examining the effect of female promiscuity on the relationship between these two traits. We found that long life makes the evolution of cooperation more likely and that promiscuous cooperative species are exceptionally long lived. These results make sense of promiscuity in cooperative breeders and clarify the importance of life-history traits in the evolution of cooperative breeding, illustrating that cooperation can evolve via the combination of indirect and direct fitness benefits.     

The impact of diapause on the evolution of other life history traits in flesh flies

Summary Flesh flies (Sarcophagidae) collected in Costa Rica and Panama lack the pupal diapause that is characteristic of flesh flies from the temperate zone and tropical Africa. The absence of a diapause capacity in the neotropical species correlates with several other life history traits: in most species the post feeding wandering phase of the third larval instar is longer and duration is more variable, adult life is longer, clutch size is smaller, and more clutches are produced. Among species that have the capacity for diapause, risk is invested primarily in the diapausing stage and other life stages are brief. Though diapausing species are short-lived, they produce as many or more progeny than nondiapausing species by increasing clutch size. The slower and more variable developmental rate and increased adult longevity desynchronizes development and permits the nondiapausing species to spread an environmental risk over different stages of the life cycle, thus offering an alternative to diapause. Other traits such as body size, developmental velocity, thermal constant thresholds, thermal constants, age at first reproduction, and the interval between clutches do not appear related to the capacity for diapause.     

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.     

Ecological constraints on the evolution of avian brains

Birds have brains that are comparable in size to those of mammals. However, variation in relative avian brain size is greater in birds. Thus, birds are ideal subjects for comparative studies on the ecological and behavioral influences on the evolution of the brain and its components. Previous studies of ecological or behavioral correlates in relative brain size were mainly based on gross comparisons between higher taxa or focussed on the relationships between the sizes of specific brain structures and the complexity of different tasks. Here we examine variation in dimensions of the braincase, relative overall brain size and size of its components, in reference to one general ecological and behavioral task: migration. We used data from three lineages of closely related species (14 Acrocephalines, 17 Sylvia and 49 parulid warblers). Within each group, species vary in their migratory tendencies. We found that species migrating long distances have lower skulls and smaller forebrains than resident species. We discuss four hypotheses that could explain smaller forebrain sizes, and suggest relevant taxa to use in comparative analyses to examine each of these hypotheses:

Ecological constraints on breeding system evolution: the influence of habitat on brood desertion in Kentish plover

1. One of the fundamental insights of behavioural ecology is that resources influence breeding systems. For instance, when food resources are plenty, one parent is able to care for the young on its own, so that the other parent can desert and became polygamous. We investigated this hypothesis in the context of classical polyandry when females may have several mates within a single breeding season, and parental duties are carried out largely by the male. 2. We studied a precocial wader, the Kentish plover Charadrius alexandrinus, that exhibits variable brood care such that the chicks may be raised by both parents, only by the female or, more often, only by the male. The timing of female desertion varies: some females desert their brood at hatching of the eggs and lay a clutch for a new mate, whereas other females stay with their brood until the chicks fledge. Kentish plovers are excellent organisms with which to study breeding system evolution, as some of their close relatives exhibit classical polyandry (Eurasian dotterel Eudromias morinellus, mountain plover Charadrius montanus), whereas others are polygynous (northern lapwing Vanellus vanellus). 3. Kentish plovers raised their broods in two habitats in our study site in southern Turkey: saltmarsh and lakeshore. Food intake was higher on the lakeshore than in the saltmarsh as judged from feeding behaviour of chicks and adults. As the season proceeded and the saltmarsh dried out, the broods moved toward the lakeshore. 4. As the density of plovers increased on lakeshore, the parents spent more time defending their young, and female parents stayed with their brood longer on the lakeshore. 5. We conclude that the influence of food abundance on breeding systems is more complex than currently anticipated. Abundant food resources appear to have profound implications on spatial distribution of broods, and the social interactions between broods constrain female desertion and polyandry.     

Seedling herbivory, community composition and plant life history traits

Despite the voluminous literature documenting plant-animal interactions, it is only recently that ecologists have begun to focus upon the importance of seedling herbivory in plant communities. This review aims to synthesize our current understanding of the effect that selective seedling removal by herbivores has in shaping post-disturbance plant community structure. In order to do this I describe how individual seedling and plant community characteristics influence the likelihood of seedling herbivory. I argue that seedling palatability, size and morphology, together with the frequency, distribution and timing of seedling emergence all play a significant role in determining seedling regeneration success in the face of herbivore attack. I also outline how current plant defence theories can be related to recent field observations concerning seedling acceptability and removal. In addition, I suggest that those seedling characteristics which provide the emerging plant with some degree of resistance against herbivory should be viewed as one component of a suite of plant life history traits affecting seedling regeneration success or failure. In view of the increasing importance of comparative methods in plant ecology, I propose that future research should integrate seedling acceptability with other plant life history traits thought to affect seedling regeneration. Recent work suggests that seed size may be paramount in determining regeneration success. I explore the possibility that seed size and seedling acceptability may be linked and discuss how these two factors may interact along successional gradients in plant communities.