Lifetime Breeding Success Research Articles

Genetic architecture of inbreeding depression may explain its persistence in a population of wild red deer.

Inbreeding depression is of major concern in declining populations, but relatively little is known about its genetic architecture in wild populations, such as the degree to which it is composed of large or small effect loci and their distribution throughout the genome. Here, we combine fitness and genomic data from a wild population of red deer to investigate the genomic distribution of inbreeding effects. Based on the runs of homozygosity (ROH)-based inbreeding coefficient, FROH, we use chromosome-specific inbreeding coefficients (FROHChr) to explore whether the effect of inbreeding varies between chromosomes. Under the assumption that within an individual the probability of being identical-by-descent is equal across all chromosomes, we used a multi-membership model to estimate the deviation of FROHChr from the average inbreeding effect. This novel approach ensures effect sizes are not overestimated whilst maximising the power of our available dataset of >3000 individuals genotyped on >35,000 autosomal SNPs. We find that most chromosomes confer a minor reduction in fitness-related traits, which when these effects are summed, results in the observed inbreeding depression in birth weight, survival and lifetime breeding success. However, no chromosomes had a significant detrimental effect compared to the overall effect of inbreeding, indicating no major effect loci. We conclude that in this population, inbreeding depression is likely the result of multiple mildly or moderately deleterious mutations spread across all chromosomes, which are difficult to detect with statistical confidence. Such mutations will be inefficiently purged, which may explain the persistence of inbreeding depression in this population.

Correlates of early reproduction and apparent fitness consequences in male Soay sheep.

Life history trade-offs are ubiquitous across species and place constraints on the timing of life history events, including the optimal age at first reproduction. However, studies on lifetime breeding success of male mammals are rare due to sex-biased dispersal and the requirement for genetic paternity inferences. We studied the correlates and apparent fitness consequences of early life reproduction among males in a free-living population of Soay sheep (Ovis aries) on St Kilda, Scotland. We investigated the factors associated with early breeding success and the apparent consequences of early success for survival and future reproduction. We used genetic paternity inferences, population data, and individual morphology measurements collected over 30 years. We found that individuals born in years with low-density population size had the highest early life breeding success and singletons were more likely to be successful than twins. Individuals that bred successfully at 7 months were more likely to survive their first winter. For individuals that survived their first winter, early breeding success was not associated with later breeding success. As individual heterogeneity affects breeding success, we believe that variation in individual quality masks the costs of early reproduction in this population. Our findings provide no evidence for selection for delayed age at reproduction in male Soay sheep.

Different proxies, different stories? Imperfect correlations and different determinants of fitness in bighorn sheep.

Measuring individual fitness empirically is required to assess selective pressures and predicts evolutionary changes in nature. There is, however, little consensus on how fitness should be empirically estimated. As fitness proxies vary in their underlying assumptions, their relative sensitivity to individual, environmental, and demographic factors may also vary. Here, using a long-term study, we aimed at identifying the determinants of individual fitness in bighorn sheep (Ovis canadensis) using seven fitness proxies. Specifically, we compared four-lifetime fitness proxies: lifetime breeding success, lifetime reproductive success, individual growth rate, individual contribution to population growth, and three multi-generational proxies: number of granddaughters, individual descendance in the next generation, and relative genetic contribution to the next generation. We found that all proxies were positively correlated, but the magnitude of the correlations varied substantially. Longevity was the main determinant of most fitness proxies. Individual fitness calculated over more than one generation was also affected by population density and growth rate. Because they are affected by contrasting factors, our study suggests that different fitness proxies should not be used interchangeably as they may convey different information about selective pressures and lead to divergent evolutionary predictions. Uncovering the mechanisms underlying variation in individual fitness and improving our ability to predict evolutionary change might require the use of several, rather than one, the proxy of individual fitness.

Exposure to Pb impairs breeding success and is associated with longer lifespan in urban European blackbirds

Although several factors have been highlighted to explain the influence of urbanization on bird fitness and survival, the role of persistent toxicants such as lead (Pb), which is typically present in urban areas worldwide, has seldom been studied despite the ecological importance of such a widespread stressor. Studying free-living European blackbirds (Turdus merula) in city parks, we tested the hypothesis that low-dose chronic exposure to Pb could shape the life-history traits of urban birds. The feather concentrations of Pb and cadmium were typical of urban areas and low-to-moderate contamination of sites. Although the lifetime breeding success of females decreased with increasing exposure to Pb, the lifespan and survival probabilities of blackbirds increased with Pb contamination regardless of gender. Breeding effort-dependent patterns in the relationship between lifespan and Pb levels were highlighted. No significant relationships were detected between cadmium and life-history traits. The results suggest a possible trade-off between self-maintenance and reproduction, with the most affected birds redirecting allocations towards their own survival, which is consistent with the “stress hormone hypothesis”. These findings suggest that Pb pollution in urban environments may shape avian ecological features and be one of the drivers of wildlife responses to urbanization and that some urban areas may function as ecological traps driven by pollutants.

Can threatened species adapt in a restored habitat? No expected evolutionary response in lay date for the New Zealand hihi.

Many bird species have been observed shifting their laying date to earlier in the year in response to climate change. However, the vast majority of these studies were performed on non‐threatened species, less impacted by reduced genetic diversity (which is expected to limit evolutionary response) as a consequence of genetic bottlenecks, drift and population isolation. Here, we study the relationship between lay date and fitness, as well as its genetic basis, to understand the evolutionary constraints on phenology faced by threatened species using a recently reintroduced population of the endangered New Zealand passerine, the hihi (Notiomystis cincta). A large discrepancy between the optimal laying date and the mode of laying date creates a strong selection differential of −11.24. The impact of this discrepancy on fitness is principally mediated through survival of offspring from hatchling to fledgling. This discrepancy does not seem to arise from a difference in female quality or a trade‐off with lifetime breeding success. We find that start of breeding season depends on female age and average temperature prior to the breeding season. Laying date is not found to be significantly heritable. Overall, our research suggests that this discrepancy is a burden on hihi fitness, which will not be resolved through evolution or phenotypic plasticity. More generally, these results show that threatened species introduced to restored habitats might lack adaptive potential and plasticity to adjust their phenology to their new environment. This constraint is also likely to limit their ability to face future challenges, including climate change.

Estimating selection on the act of inbreeding in a population with strong inbreeding depression.

Inbreeding depression is widely regarded as a driving force in the evolution of dispersal, mate choice and sperm selection. However, due to likely costs of inbreeding avoidance, which are poorly understood, it is unclear to what extent selection to avoid inbreeding is expected in nature. Moreover, there are currently very few empirical estimates of the strength of selection against the act of inbreeding (mating with a relative), as opposed to the fitness costs of being inbred. Here, we use data from the individual‐based study of red deer on the Scottish island of Rum, a strongly polygynous system which harbours a large inbreeding load, to estimate selection against the act of inbreeding for each sex. We use pedigree and genomic estimates of relatedness between individuals and measure fitness using both lifetime breeding success (number of calves born) and lifetime reproductive success (number of calves surviving to independence), with the latter incorporating inbreeding depression in calf survival. We find for both sexes that the repeatability of the act of inbreeding was low (< 0.1), suggesting little among‐individual variation for this trait on which selection can act. Using the genomic measures, there was significant selection against the act of inbreeding in males, but not in females, and there was considerable uncertainty in the estimate in both sexes. We discuss possible explanations for these patterns and their implications for understanding the evolution of inbreeding avoidance in natural populations.

Determinants of age at first reproduction and lifetime breeding success revealed by full paternity assignment in a male ungulate

Age at first reproduction is an important determinant of individual variation in reproductive success in ungulates, but few studies have examined its relationship with later fitness‐related traits in males. We used a long‐term individual based study of a harvested moose population to quantify the individual reproductive performance and survival of males, as well as to examine the determinants of age at first reproduction and consequences of age at first reproduction on lifetime breeding success. The probability that a male successfully reproduced at the age of two was negatively related to the mean age of adult males in the population, but the relationship weakened with increasing population size. Large antlers and large body mass relative to other males in the population increased the number of calves sired at their first successful mating season. In addition, those that successfully reproduced as two year‐olds were more likely to sire calves the next year, making them more productive at a given age compared to those that first reproduced at the age of three or older. We emphasize the importance for males to start reproducing as soon as possible in a harvested population to gain lifetime fitness benefits, as surviving the hunt is a major determinant of reproductive success in this population. We found no costs of early reproduction in males, hence leading to high individual heterogeneity in male reproductive performance. The apparent lack of reproductive costs could partly be explained by the age distribution in the population, individual variation in early‐life body mass and antler size, and differences in probabilities of being hunted of successful and unsuccessful males.

Occupancy time in sets of states for demographic models

As an individual moves through its life cycle, it passes through a series of states (age classes, size classes, reproductive states, spatial locations, health statuses, etc.) before its eventual death. The occupancy time in a state is the time spent in that state over the individual’s life. Depending on the life cycle description, the occupancy times describe different demographic variables, for example, lifetime breeding success, lifetime habitat utilisation, or healthy longevity.Models based on absorbing Markov chains provide a powerful framework for the analysis of occupancy times. Current theory, however, can completely analyse only the occupancy of single states, although the occupancy time in a set of states is often desired. For example, a range of sizes in a size-classified model, an age class in an age×stage model, and a group of locations in a spatial stage model are all sets of states.We present a new mathematical approach to absorbing Markov chains that extends the analysis of life histories by providing a comprehensive theory for the occupancy of arbitrary sets of states, and for other demographic variables related to these sets (e.g., reaching time, return time). We apply this approach to a matrix population model of the Southern Fulmar (Fulmarus glacialoides). The analysis of this model provides interesting insight into the lifetime number of breeding attempts of this species.Our new approach to absorbing Markov chains, and its implementation in matrix oriented software, makes the analysis of occupancy times more accessible to population ecologists, and directly applicable to any matrix population models.

Comparative studies need to rely both on sound natural history data and on excellent statistical analysis.

We certainly agree with Schradin [1] that comparative studies need to use the best information available—as well as clear definitions, up-to-date statistical techniques and common sense. We have divided our response into two sections: the first dealing with Schradin's critique of our 2017 paper and the classification of the social organization of shrews; the second dealing with three general issues that his commentary raises. The paper that Schradin is commenting on [2] asks whether cooperative breeders (which we define as species where non-breeding helpers assist breeders to raise their young) in mammals are more commonly found in arid environments than monogamous species (defined as species where breeding pairs of males and females remain together for more than one season) from which cooperative breeders appear to be derived [3]. It shows that, as in birds, cooperative breeders tend to live in relatively arid habitats compared to monogamous species. As we describe below, these conclusions are unaffected by differences between our classification of the social organization of shrews and the classification suggested by Schradin. Schradin's first criticism is that the categorizations of shrews that we have used in this analysis were based on one paper on a single species. This is incorrect, for our categorization of shrews was based on more than 70 separate sources (see electronic supplementary material, appendix S1). When we published our dataset [4], we were required to reduce the associated reference list by the editors of the journal and, to comply, we removed around 75% of our 2000+ sources, often listing a single reference per species or group of species, and frequently using generic reviews for particular groups where these were available: for example, for many rodent species, we simply listed Wolff and Sherman's Rodent Societies [5], and …

Endocranial volume is heritable and is associated with longevity and fitness in a wild mammal.

Research on relative brain size in mammals suggests that increases in brain size may generate benefits to survival and costs to fecundity: comparative studies of mammals have shown that interspecific differences in relative brain size are positively correlated with longevity and negatively with fecundity. However, as yet, no studies of mammals have investigated whether similar relationships exist within species, nor whether individual differences in brain size within a wild population are heritable. Here we show that, in a wild population of red deer (Cervus elaphus), relative endocranial volume was heritable (h2 = 63%; 95% credible intervals (CI) = 50–76%). In females, it was positively correlated with longevity and lifetime reproductive success, though there was no evidence that it was associated with fecundity. In males, endocranial volume was not related to longevity, lifetime breeding success or fecundity.

Age-related effects on breeding phenology and success of Common Guillemots Uria aalge at a North Sea colony

ABSTRACTCapsule: Common Guillemots Uria aalge show delayed breeding and marked age-related changes in reproductive success consistent with improved performance with experience.Aims: To determine age of first breeding and age-related effects on breeding phenology and success of Common Guillemots.Methods: Resighting data from a long-term colour-ringing study of Common Guillemot chicks were combined with observations of breeding phenology and success to follow the recruitment process, breeding phenology and success of 62 birds at a major North Sea colony over a 30-year period.Results: The median age of first breeding of Common Guillemots was 6.6 years. There were no detectable costs of first breeding on return rates or the likelihood of breeding the next season but first time breeders bred later and less successfully. Age of first breeding and lifetime breeding success both varied among individuals but there was no clear optimal age of first breeding and early first breeding was not associated with higher lifetime breeding success.Conclusions: Common Guillemots in the Isle of May population delayed breeding for 3–4 years beyond physiological maturity. The marked increase in breeding success with age was consistent with improved performance with experience rather than selection for higher quality individuals. Findings from this study will inform population models by providing improved estimates of age of first breeding and age-related changes in reproductive performance.

Natural selection on individual variation in tolerance of gastrointestinal nematode infection.

Author SummaryAnimals can defend themselves against parasites through either resistance (reducing parasite numbers, for example, by killing them) or tolerance (maintaining health as infections levels increase, for example, by repairing damage). Resistance has been well-studied in wild animals, but tolerance has been less so. We analysed data on body weight collected over 25 years on a natural population of Soay sheep, infected with parasitic gut worms. As parasite burden increased, sheep lost weight. Crucially, there was variation among individuals: some lost weight rapidly with increasing infections (i.e., showed “low tolerance”), whereas others lost weight slowly (i.e., showed “high tolerance”). The least tolerant individuals lost 4.5 kg of body weight across the range of parasite burdens that we saw, whereas the most tolerant lost only around 0.36 kg. However, variation in tolerance did not have a heritable genetic basis, so that although tolerance varied between individuals, this was not due to genetic differences. Further analysis revealed that there was natural selection on tolerance. Individuals who were more tolerant of infection produced more offspring over the course of their lives. This study shows that natural selection can act upon resistance and tolerance simultaneously in nature, a result that has implications for both human health and livestock management.

Costs of mating competition limit male lifetime breeding success in polygynous mammals.

Although differences in breeding lifespan are an important source of variation in male fitness, the factors affecting the breeding tenure of males have seldom been explored. Here, we use cross-species comparisons to investigate the correlates of breeding lifespan in male mammals. Our results show that male breeding lifespan depends on the extent of polygyny, which reflects the relative intensity of competition for access to females. Males have relatively short breeding tenure in species where individuals have the potential to monopolize mating with multiple females, and longer ones where individuals defend one female at a time. Male breeding tenure is also shorter in species in which females breed frequently than in those where females breed less frequently, suggesting that the costs of guarding females may contribute to limiting tenure length. As a consequence of these relationships, estimates of skew in male breeding success within seasons overestimate skew calculated across the lifetime and, in several polygynous species, variance in lifetime breeding success is not substantially higher in males than in females.

Early reproductive investment, senescence and lifetime reproductive success in femaleAsian elephants

The evolutionary theory of senescence posits that as the probability of extrinsic mortality increases with age, selection should favour early-life over late-life reproduction. Studies on natural vertebrate populations show early reproduction may impair later-life performance, but the consequences for lifetime fitness have rarely been determined, and little is known of whether similar patterns apply to mammals which typically live for several decades. We used a longitudinal dataset on Asian elephants (Elephas maximus) to investigate associations between early-life reproduction and female age-specific survival, fecundity and offspring survival to independence, as well as lifetime breeding success (lifetime number of calves produced). Females showed low fecundity following sexual maturity, followed by a rapid increase to a peak at age 19 and a subsequent decline. High early life reproductive output (before the peak of performance) was positively associated with subsequent age-specific fecundity and offspring survival, but significantly impaired a female's own later-life survival. Despite the negative effects of early reproduction on late-life survival, early reproduction is under positive selection through a positive association with lifetime breeding success. Our results suggest a trade-off between early reproduction and later survival which is maintained by strong selection for high early fecundity, and thus support the prediction from life history theory that high investment in reproductive success in early life is favoured by selection through lifetime fitness despite costs to later-life survival. That maternal survival in elephants depends on previous reproductive investment also has implications for the success of (semi-)captive breeding programmes of this endangered species.

The effect of socio-economic status and food availability on first birth interval in a pre-industrial human population

Individual variation in nutritional status has direct implications for fitness and thus is crucial in shaping patterns of life-history variation. Nevertheless, it is difficult to measure in natural populations, especially in humans. Here, we used longitudinal data on individual life-histories and annual crop yield variation collected from pre-industrial Finnish populations experiencing natural mortality and fertility to test the validity of first birth interval (FBI; time between marriage and first birth) as a surrogate measure of nutritional status. We evaluated whether women with different socio-economic groups differ in length of FBI, whether women of poorer socio-economic status and experiencing lower crop yields conceive slower following marriage, and whether shorter FBI is associated with higher lifetime breeding success. We found that poorer women had longer FBI and reduced probability of giving birth in months with low food availability, while the FBI of richer women was not affected by variation in food availability. Women with shorter FBI achieved higher lifetime breeding success and a faster reproductive rate. This is, to our knowledge, the first study to show a direct relationship between environmental conditions and speed of childbirth following marriage, highlighting the value of FBI as an indicator of nutritional status when direct data are lacking.

Shared spatial effects on quantitative genetic parameters: accounting for spatial autocorrelation and home range overlap reduces estimates of heritability in wild red deer.

Social structure, limited dispersal, and spatial heterogeneity in resources are ubiquitous in wild vertebrate populations. As a result, relatives share environments as well as genes, and environmental and genetic sources of similarity between individuals are potentially confounded. Quantitative genetic studies in the wild therefore typically account for easily captured shared environmental effects (e.g., parent, nest, or region). Fine-scale spatial effects are likely to be just as important in wild vertebrates, but have been largely ignored. We used data from wild red deer to build “animal models” to estimate additive genetic variance and heritability in four female traits (spring and rut home range size, offspring birth weight, and lifetime breeding success). We then, separately, incorporated spatial autocorrelation and a matrix of home range overlap into these models to estimate the effect of location or shared habitat on phenotypic variation. These terms explained a substantial amount of variation in all traits and their inclusion resulted in reductions in heritability estimates, up to an order of magnitude up for home range size. Our results highlight the potential of multiple covariance matrices to dissect environmental, social, and genetic contributions to phenotypic variation, and the importance of considering fine-scale spatial processes in quantitative genetic studies.

Male greater sac-winged bats gain direct fitness benefits when roosting in multimale colonies

Social groups that are characterized by the presence of male kin are rare in mammals. Theory predicts that males reproducing in such groups need to overcome the costs of local mate competition, which are supposedly severe in polygynous or promiscuous mating systems. Here, we studied in a polygynous mammal with male philopatry whether male group size renders direct fitness benefits for males that could outweigh the costs of competing with related males for access to territories and mates. We used long-term behavioral observations and genetic data of the greater sac-winged bat to investigate the factors affecting lifetime breeding success (LBS) of harem males living in colonies that contain varying numbers of male residents. We show that tenure of harem males increased with the number of male coresidents and that harem male tenure explained a large proportion of variation in their LBS. Thus, our results provide evidence that males gain direct fitness benefits from a social organization in colonies that include additional harem territories and nonharem males. Immigration of males into colonies was significantly lower when nonharem males (young males that are often related to harem males) were permanently present in colonies, suggesting that larger male groups may be better able to maintain a patriline in a colony and thus also ensure future indirect fitness benefits. Key words: female-biased dispersal, lifetime breeding success, male tenure, Saccopteryx bilineata, social organization. [Behav Ecol]

Alloparental behaviour and long-term costs of mothers tolerating other members of the group in a plurally breeding mammal

Cooperative-breeding studies tend to focus on a few alloparental behaviours in highly cooperative species exhibiting high reproductive skew and the associated short-term, but less frequently long-term, fitness costs. We analysed a suite of alloparental behaviours (assessed via filming) in a kin-structured, high-density population of plurally breeding European badgers, Meles meles, which are not highly cooperative. Group members, other than mothers, performed alloparental behaviour; however, this was not correlated with their relatedness to within-group young. Furthermore, mothers babysat, allogroomed cubs without reciprocation, and allomarked cubs more than other members of the group (controlling for observation time). For welfare reasons, we could not individually mark cubs; however, the number observed pre-independence never exceeded that trapped. All 24 trapped cubs, in three filmed groups, were assigned both parents using 22 microsatellites. Mothers may breed cooperatively, as the time they babysat their assigned, or a larger, litter size did not differ. Furthermore, two mothers probably allonursed, as they suckled more cubs than their assigned litter size. An 18-year genetic pedigree, however, detected no short-term (litter size; maternal survival to the following year) or long-term (offspring breeding probability; offspring lifetime breeding success) fitness benefits with more within-group mothers or other members of the group. Rather, the number of other members of the group (excluding mothers) correlated negatively with long-term fitness. Mothers may tolerate other members of the group, as nonbreeders undertook more digging. Our study highlights that alloparental care varies on a continuum from that seen in this high-density badger population, where alloparenting behaviour is minimal, through to species where alloparental care is common and provides fitness benefits.

Fitness measures in selection analyses: sensitivity to the overall number of offspring produced in a lifetime

Age at first (alpha) and last (omega) breeding are important life-history traits; however, the direction and strength of selection detected on traits may vary depending on the fitness measure used. We provide the first estimates of lifetime breeding success (LBS) and lambda(ind) (the population growth rate of an individual) of European badgers Meles meles, by genotyping 915 individuals, sampled over 18 years, for 22 microsatellites. Males are slightly larger than females, and the opportunity for selection was slightly greater for males, as predicted. lambda(ind) and LBS both performed well in predicting the number of grand-offspring, and both detected selection for a late omega, until the age of eight. Differential selection (S'(alpha)) for an early alpha, however, was only detected using LBS, not with lambda(ind). In declining populations (lambda(ind) < 1) selection favours reproduction later in life, whereas early reproduction is selected in increasing populations (lambda(ind) > 1). As 41% of badgers were assigned only one offspring (lambda(ind) < 1), whereas 40% were assigned more than two (lambda(ind) > 1), this cancelled out S'(alpha) measured by lambda(ind).

Sexual conflict in twins: male co-twins reduce fitness of female Soay sheep

Males and females often have different requirements during early development, leading to sex-specific interactions between developing offspring. In polytocous mammals, competition for limited resources in utero may be asymmetrical between the sexes, and androgens produced by male foetuses could have adverse effects on the development of females, with potentially long-lasting consequences. We show here, in an unmanaged population of Soay sheep, that female lambs with a male co-twin have reduced birth weight relative to those with a female co-twin, while there was no such effect in male twins. In addition, females with a male co-twin had lower lifetime breeding success, which appeared to be mainly driven by differences in first-year survival. These results show that sex-specific sibling interactions can have long-term consequences for survival and reproduction, with potentially important implications for optimal sex allocation.