The carryover effects of embryonic incubation temperature on subsequent growth and thermal tolerance in white sturgeon.

Environmental variation experienced during early periods of development can lead to persistent phenotypic alteration, known as carryover effects. Such effects increase concern for threatened or endangered species such as the white sturgeon (Acipenser transmontanus), particularly considering expected thermal changes due to climate change. We evaluated how temperature during embryonic development affects physiological parameters such as larval and early juvenile growth and thermal tolerance. Nechako River white sturgeon embryos were incubated at different environmental temperatures (Te) of 12 °C (the natural spawning temperature of this population), 15 °C (the hatchery incubation temperature), and 18 °C (representing potential increases in river temperatures given global climate change). After hatch, fish were reared at a common 15 °C for 80 days post-hatch (dph). Individuals from each temperature treatment were tested for thermal tolerance using the critical thermal maximum method (CTmax), euthanized, and measured. Fish were examined at regular intervals from 13 to 80 dph, which bridged the time from the start of exogenous feeding through the transition into early juveniles. We found carryover effects of high embryonic Te in the short term for both thermal tolerance and growth. Fish that developed at 18 °C had the lowest thermal tolerance during the start of exogenous feeding. However, differences in thermal tolerance were small for early juveniles and were unlikely to be ecologically relevant in the longer term. Fish that developed at 18 °C were smallest over the observation period, indicating a possible cost for survival from increasing environmental temperatures during embryonic development. This research represents a window into a critical period of development during which fish are particularly vulnerable to climatic variation, and shows that cooler temperatures (12 °C) during incubation are optimal for this population. The results can inform environmental managers on the best strategies to help conserve current white sturgeon populations across their range.

Immune genotypes, immune responses, and survival in a wild bird population.

Individuals vary in their immune genotype, inbreeding coefficient f, immune responses, survival to adulthood, and adult longevity. However, whether immune genes predict survival or longevity, whether such relationships are mediated through immune responses, and how f affects immune genotype remain unclear. We use a wild song sparrow (Melospiza melodia) population in which survival to adulthood, adult longevity, and f were measured precisely, and in which immune responses have previously been assessed. We investigate four toll-like receptor (TLR) and the major histocompatibility complex (MHC) class IIB exon 2 genes. We test whether immune genes predict fitness (survival to adulthood or adult longevity); whether immune genes predict immune response; whether immune response predicts fitness and whether fitness, immune responses, or immune genotypes are correlated with f. We find that survival to adulthood is not associated with immune gene variation, but adult longevity is decreased by high MHC allele diversity (especially in birds that were relatively outbred), and by the presence of a specific MHC supertype. Immune responses were affected by specific immune genotypes. Survival to adulthood and adult longevity were not predicted by immune response, implying caution in the use of immune response as a predictor for fitness. We also found no relationship between f and immune genotype. This finding indicates that immune gene associations with longevity and immune response are not artefacts of f, and suggests that pathogen-mediated selection at functional loci can slow the loss of genetic variation arising from genetic drift and small population size.

Kidnapping intergroup young: an alternative strategy to maintain group size in the group-living pied babbler (Turdoides bicolor).

Both inter- and intragroup interactions can be important influences on behaviour, yet to date most research focuses on intragroup interactions. Here, we describe a hitherto relatively unknown behaviour that results from intergroup interaction in the cooperative breeding pied babbler: kidnapping. Kidnapping can result in the permanent removal of young from their natal group. Since raising young requires energetic investment and abductees are usually unrelated to their kidnappers, there appears no apparent evolutionary advantage to kidnapping. However, kidnapping may be beneficial in species where group size is a critically limiting factor (e.g. for reproductive success or territory defence). We found kidnapping was a highly predictable event in pied babblers: primarily groups that fail to raise their own young kidnap the young of others, and we show this to be the theoretical expectation in a model that predicts kidnapping to be facultative, only occurring in those cases where an additional group member has sufficient positive impact on group survival to compensate for the increase in reproductive competition. In babblers, groups that failed to raise young were also more likely to accept extragroup adults (hereafter rovers). Groups that fail to breed may either (i) kidnap intergroup young or (ii) accept rovers as an alternative strategy to maintain or increase group size. This article is part of the theme issue 'Intergroup conflict across taxa'.

Kinship, dear enemies, and costly combat: The effects of relatedness on territorial overlap and aggression in a cooperative breeder.

Many species maintain territories, but the degree of overlap between territories and the level of aggression displayed in territorial conflicts can vary widely, even within species. Greater territorial overlap may occur when neighboring territory holders are close relatives. Animals may also differentiate neighbors from strangers, with more familiar neighbors eliciting less-aggressive responses during territorial conflicts (the "dear enemy" effect). However, research is lacking in how both kinship and overlap affect territorial conflicts, especially in group-living species. Here, we investigate kinship, territorial overlap, and territorial conflict in a habituated wild population of group-living cooperatively breeding birds, the southern pied babbler Turdoides bicolor. We find that close kin neighbors are beneficial. Territories overlap more when neighboring groups are close kin, and these larger overlaps with kin confer larger territories (an effect not seen for overlaps with unrelated groups). Overall, territorial conflict is costly, causing significant decreases in body mass, but conflicts with kin are shorter than those conducted with nonkin. Conflicts with more familiar unrelated neighbors are also shorter, indicating these neighbors are "dear enemies." However, kinship modulates the "dear enemy" effect; even when kin are encountered less frequently, kin elicit less-aggressive responses, similar to the "dear enemy" effect. Kin selection appears to be a main influence on territorial behavior in this species. Groups derive kin-selected benefits from decreased conflicts and maintain larger territories when overlapping with kin, though not when overlapping with nonkin. More generally, it is possible that kinship extends the "dear enemy" effect in animal societies.

Purifying Selection in the Toll-Like Receptors of Song Sparrows Melospiza melodia.

Variation in immune gene sequences is known to influence resistance to infectious diseases and parasites, and hence survival and mate choice, across animal taxa. Toll-like receptors (TLRs) comprise one essential gene family in the vertebrate innate immune system and recognize evolutionarily conserved structures from all major microorganism classes. However, the causes and consequences of TLR variation in passerine birds remain largely unexplored. We examined 7 TLR genes in song sparrows (Melospiza melodia), a species that is studied across North America. We then examined sequences from 4 unduplicated TLRs (TLR1LB, TLR3, TLR4, and TLR15) from birds in 2 parts of the species' range (N = 27, N = 6), tested for evidence of selection, and conducted pilot analyses of the role of TLR heterozygosity in survival. We identified 45 SNPs: 19 caused changes in amino acid sequences and 2 of these were likely deleterious. We found no evidence of codon-level episodic positive selection but detected purifying selection at codons in all TLRs. Contrary to expectations we found no strong correlation between heterozygosity at TLRs and inbreeding coefficient f (estimate ± standard error [SE] = -0.68 ± 0.37, Radj2 = 0.08, F1,25 = 3.38, P = 0.08). In addition, pilot analyses revealed no relationship between TLR heterozygosity and survival (ß ± SE: 0.09 ± 2.00, P = 0.96), possibly due to small sample size. Further analyses of genetic diversity in TLRs are likely to advance understanding of the effects of innate immune gene diversity on the fitness and persistence of wild populations.

Sex differences in the drivers of reproductive skew in a cooperative breeder.

Many cooperatively breeding societies are characterized by high reproductive skew, such that some socially dominant individuals breed, while socially subordinate individuals provide help. Inbreeding avoidance serves as a source of reproductive skew in many high-skew societies, but few empirical studies have examined sources of skew operating alongside inbreeding avoidance or compared individual attempts to reproduce (reproductive competition) with individual reproductive success. Here, we use long-term genetic and observational data to examine factors affecting reproductive skew in the high-skew cooperatively breeding southern pied babbler (Turdoides bicolor). When subordinates can breed, skew remains high, suggesting factors additional to inbreeding avoidance drive skew. Subordinate females are more likely to compete to breed when older or when ecological constraints on dispersal are high, but heavy subordinate females are more likely to successfully breed. Subordinate males are more likely to compete when they are older, during high ecological constraints, or when they are related to the dominant male, but only the presence of within-group unrelated subordinate females predicts subordinate male breeding success. Reproductive skew is not driven by reproductive effort, but by forces such as intrinsic physical limitations and intrasexual conflict (for females) or female mate choice, male mate-guarding and potentially reproductive restraint (for males). Ecological conditions or "outside options" affect the occurrence of reproductive conflict, supporting predictions of recent synthetic skew models. Inbreeding avoidance together with competition for access to reproduction may generate high skew in animal societies, and disparate processes may be operating to maintain male vs. female reproductive skew in the same species.

Individual dispersal delays in a cooperative breeder: Ecological constraints, the benefits of philopatry and the social queue for dominance.

Delayed dispersal is a key step in the evolution of familial animal societies and cooperative breeding. However, no consensus has been reached on the ecological and social circumstances driving delayed dispersal. Here, we test predictions from the ecological constraints and benefits of philopatry hypotheses as well as the recently proposed dual benefits hypothesis to better understand the evolution of group-living and cooperative breeding. Furthermore, we consider how individual social circumstances within groups affect dispersal decisions. We examine 11 years of life-history information on a wild population of cooperatively breeding southern pied babblers Turdoides bicolor. We investigate the effects of ecological conditions, natal-group membership and individual social context on male and female dispersal delays, disperser survival and acquisition of dominance. Female dispersal decisions are generally unconstrained by ecological or social circumstances. In contrast, males disperse in response to relaxed ecological constraints, decreases in nepotistic tolerance or when low social rank in the queue for dominance decreases their likelihood of gaining a dominant breeding position. Early dispersal by end-of-queue males often leads to a head-of-queue subordinate position in a non-natal group, thereby increasing access to dominant breeding positions. However, males and females remaining in natal groups gain benefits of philopatry via increased survival and, for head-of-queue males, very high likelihood of acquisition of a breeding position. Overall, predictions from the dual benefits hypothesis best describe these results, while some predictions from each of the ecological constraints and benefits of philopatry hypotheses were supported. The benefits of living and working together (collective action benefits) in large stable groups are of central importance in shaping dispersal delays in southern pied babbler societies. In addition, position in the subordinate social queue for dominance is the key in determining access to reproduction, particularly for males. This research highlights the importance of considering the costs and benefits of individual social circumstances in dispersal decisions and illustrates how the dual benefits hypothesis offers new perspectives in understanding delayed dispersal.

Nepotism and subordinate tenure in a cooperative breeder.

In many cooperatively breeding societies, subordinate individuals delay dispersal and independent breeding. The length of time that subordinates delay dispersal (subordinate tenure) is likely to have important implications for both subordinate and dominant fitness. However, quantitative comparisons of the subordinate tenure of males and females are rare, especially with respect to the presence of same- versus opposite-sex close kin. Here, we investigate subordinate tenure and how it is affected by the genetic relationship between subordinates and dominants in the cooperatively breeding southern pied babbler (Turdoides bicolor). We find that for males, longer subordinate tenures result in increased likelihood of attaining dominance. In the presence of an unrelated dominant male, tenure of subordinate males is significantly shorter, indicating nepotism among males. Female tenures are unaffected by the genetic relationship to either the dominant male or female. These results are some of the first to demonstrate that the sex of both the dominants and subordinates, and the genetic relationship between them, can have significant impacts on subordinate tenure and dispersal delays. Nepotism has likely played a vital role in the evolution of cooperative breeding in this species.

Costly reproductive competition between females in a monogamous cooperatively breeding bird.

In many cooperatively breeding societies, only a few socially dominant individuals in a group breed, reproductive skew is high, and reproductive conflict is common. Surprisingly, the effects of this conflict on dominant reproductive success in vertebrate societies have rarely been investigated, especially in high-skew societies. We examine how subordinate female competition for breeding opportunities affects the reproductive success of dominant females in a monogamous cooperatively breeding bird, the Southern pied babbler (Turdoides bicolor). In this species, successful subordinate reproduction is very rare, despite the fact that groups commonly contain sexually mature female subordinates that could mate with unrelated group males. However, we show that subordinate females compete with dominant females to breed, and do so far more often than expected, based on the infrequency of their success. Attempts by subordinates to obtain a share of breeding impose significant costs on dominant females: chicks fledge from fewer nests, more nests are abandoned before incubation begins, and more eggs are lost. Dominant females appear to attempt to reduce these costs by aggressively suppressing potentially competitive subordinate females. This empirical evidence provides rare insight into the nature of the conflicts between females and the resultant costs to reproductive success in cooperatively breeding societies.

Inbreeding avoidance mechanisms: dispersal dynamics in cooperatively breeding southern pied babblers.

1. Breeding with kin can reduce individual fitness through the deleterious effects of inbreeding depression. Inbreeding avoidance mechanisms are expected to have developed in most species, and especially in cooperatively breeding species where individuals may delay dispersal until long after sexual maturity. Such potential mechanisms include sex-biased dispersal and avoidance of kin known through associative learning. 2. The investigation of inbreeding avoidance through dispersal dynamics can be enhanced by combining fine-scale population genetic structure data with detailed behavioural observations of wild populations. 3. We investigate possible inbreeding avoidance in a wild population of cooperatively breeding southern pied babblers (Turdoides bicolor). A combination of genetic, geographic and observational data is used to examine fine-scale genetic structure, dispersal (including sex-biased dispersal) and inheritance of dominance in cooperatively breeding groups. 4. Unusually, sex-bias in dispersal distance does not occur. Rather, individuals appear to avoid inbreeding through two routes. First, through dispersal itself: although both males and females disperse locally, they move outside the range within which genetically similar individuals are usually found, going twice as far from natal groups as from non-natal groups. Second, through avoidance of familiar group members as mates: individuals inherit a dominant position in the natal group only when an unrelated breeding partner is present. 5. This study uses spatial genetic analyses to investigate inbreeding avoidance mechanisms in a cooperative breeder and shows that individuals of both sexes can avoid inbreeding through a dispersal distance mechanism. While it appears that dispersal allows most individuals to move beyond the range of closely related kin, matings may still occur between distant kin. Nevertheless, any costs of breeding with a distant relative may be outweighed by the benefits of local dispersal and the immense fitness gains available from attaining a breeding position.

Synchronous provisioning increases brood survival in cooperatively breeding pied babblers.

1. Behavioural synchrony typically involves trade-offs. In the context of foraging, for example, synchrony may be suboptimal when individuals have different energy requirements but yield net benefits in terms of increased foraging success or decreased predation risk. 2. Behavioural synchrony may also be advantageous when individuals collaborate to achieve a common goal, such as raising young. For example, in several bird species, provisioners synchronize nest-feeding visits. However, despite the apparent prevalence of provisioning synchrony, it is not known whether it is adaptive or what its function might be. 3. Here, we propose a novel explanation for provisioning synchrony: it increases brood survival by decreasing the number of temporally separate nest visits and accordingly the chance that the nest will be detected by predators. Using cooperatively breeding pied babblers, we showed experimentally that provisioners synchronized nest visits by waiting for another provisioner before returning to the nest. Brood survival increased with provisioning synchrony. Provisioners were more likely to synchronize feeding visits for older nestlings as they were louder and possibly more conspicuous to predators. Finally, provisioners in large groups were more likely to wait for other provisioners and synchronized a higher proportion of all visits than those in smaller groups. Thus, provisioning synchrony may be one mechanism by which large groups increase brood survival in this species. 4. This study highlights a novel strategy that birds use to increase the survival of young and demonstrates the advantages of coordinated behaviour in social species.