Lifetime Reproductive Success Research Articles

More than mortality: Consequences of human activity on migrating birds extend beyond direct mortality

AbstractBirds must contend with an array of anthropogenic threats during their migratory journeys. Many migrants are killed due to encounters with artificial light, introduced species, pollutants, and other anthropogenic hazards, while survivors of these encounters can suffer longer-lasting negative effects. The nonlethal effects of anthropogenic threats on migrating birds are less well understood than direct mortality, yet both potentially contribute to population declines. For example, building collisions frequently kill migrating birds, but the numbers of migrants that survive with an impaired ability to fly, refuel, or navigate to their destination on time is not well understood. Though not immediately fatal, such injuries can lead to delayed mortality and, ultimately, reduced lifetime reproductive success. Furthermore, migrants are likely to encounter multiple threats on their journeys, which can interact synergistically to further reduce fitness. For instance, light pollution attracts and disorients migrants, increasing the likelihood of window strikes, and surviving birds may be more vulnerable to predation from introduced predators. While considerable attention has focused on the lethal effects of anthropogenic threats, here, we review nonlethal effects of eight types of threats during migration, their interactions, and the pathways through which they can exert fitness costs. In doing so, we identify knowledge gaps and suggest areas for future research. In the absence of more information, we propose that the greatest reduction in the cumulative lethal and nonlethal impacts of anthropogenic hazards will be achieved by addressing threat types, like artificial light at night, that interact with and compound the impact of additional threats. Direct mortality from anthropogenic sources is recognized as a key driver of population declines, but a full understanding of the impacts of human activity on migrating birds must include the cumulative and interacting effects that extend beyond immediate mortality en route to influence overall migration success and lifetime fitness.

Hurricanes affect diversification among individual life courses of a primate population.

Extreme climatic events may influence individual-level variability in phenotypes, survival and reproduction, and thereby drive the pace of evolution. Climate models predict increases in the frequency of intense hurricanes, but no study has measured their impact on individual life courses within animal populations. We used 45 years of demographic data of rhesus macaques to quantify the influence of major hurricanes on reproductive life courses using multiple metrics of dynamic heterogeneity accounting for life course variability and life-history trait variances. To reduce intraspecific competition, individuals may explore new reproductive stages during years of major hurricanes, resulting in higher temporal variation in reproductive trajectories. Alternatively, individuals may opt for a single optimal life-history strategy due to trade-offs between survival and reproduction. Our results show that heterogeneity in reproductive life courses increased by 4% during years of major hurricanes, despite a 2% reduction in the asymptotic growth rate due to an average decrease in mean fertility and survival by that is, shortened life courses and reduced reproductive output. In agreement with this, the population is expected to achieve stable population dynamics faster after being perturbed by a hurricane ( ; 95% CI: 1.488, 1.538), relative to ordinary years . Our work suggests that natural disasters force individuals into new demographic roles to potentially reduce competition during unfavourable environments where mean reproduction and survival are compromised. Variance in lifetime reproductive success and longevity are differently affected by hurricanes, and such variability is mostly driven by survival.

Early-life telomere length predicts life-history strategy and reproductive senescence in a threatened wild songbird.

Telomeres are well known for their associations with lifespan and ageing across diverse taxa. Early-life telomere length can be influenced by developmental conditions and has been shown positively affect lifetime reproductive success in a limited number of studies. Whether these effects are caused by a change in lifespan, reproductive rate or perhaps most importantly reproductive senescence is unclear. Using long-term data on female breeding success from a threatened songbird (the hihi, Notiomystis cincta), we show that the early-life telomere length of individuals predicts the presence and rate of future senescence of key reproductive traits: clutch size and hatching success. In contrast, senescence of fledging success is not associated with early-life telomere length, which may be due to the added influence of biparental care at this stage. Early-life telomere length does not predict lifespan or lifetime reproductive success in this species. Females may therefore change their reproductive allocation strategy depending on their early developmental conditions, which we hypothesise are reflected in their early-life telomere length. Our results offer new insights on the role that telomeres play in reproductive senescence and individual fitness and suggest telomere length can be used as a predictor for future life history in threatened species.

Thelong-lasting legacy of reproduction: lifetime reproductive success shapes expected genetic contributions of humansafter 10 generations.

An individual's lifetime reproductive success (LRS) measures its realized genetic contributions to the next generation, but how well does it predict this over longer periods? Here we use human genealogical data to estimate expected individual genetic contributions (IGC) and quantify the degree to which LRS, relative to other fitness proxies, predicts IGC over longer periods. This allows an identification of the life-history stages that are most important in shaping variation in IGC. We use historical genealogical data from two non-isolated local populations in Switzerland to estimate the stabilized IGC for 2230 individuals approximately 10 generations after they were born. We find that LRS explains 30% less variation in IGC than the best predictor of IGC, the number of grandoffspring. However, albeit less precise than the number of grandoffspring, we show that LRS does provide an unbiased prediction of IGC. Furthermore, it predicts IGC better than lifespan, and accounting for offspring survival to adulthood does not improve the explanatory power. Overall, our findings demonstrate the value of human genealogical data to evolutionary biology and suggest that reproduction-more than lifespan or offspring survival-impacts the long-term genetic contributions of historic humans, even in a population with appreciable migration.

Reproductive Success Dynamics Could Limit Precision in Close-Kin Mark–Recapture Abundance Estimation for Atlantic Goliath Grouper (Epinephelus itajara)

Extra-Poisson variance in annual reproductive success can affect the precision of abundance estimates made using ‘close-kin’ mark–recapture procedures. However, empirical evaluation of that variance in natural marine populations can be daunting. Here, a scaling method was used to extend a discrete-time, age-structured model, facilitating investigation of annual and lifetime reproductive success dynamics in Epinephelus itajara. Life tables were synthesized from fishery assessment vital rates and life history measures. For model scaling, a precise empirical estimate of effective population size for the studied population was utilized as the independent variable, and model sensitivity to an informative range of adult abundance was evaluated. The potential for sex reversal to impact reproductive success dynamics was also investigated, albeit in the absence of selective fishing pressure and potential compensatory or depensatory responses. Close-kin relationships in a genetic sample of ~300 adults collected from spawning sites in the Florida Atlantic included numerous full-sibling pairs and multi-sibling families, which is unusual for long-lived, iteroparous marine populations with broadly dispersed larvae. The highly overdispersed reproductive success dynamics modeled for this population and its atypical kinship distribution could have ramifications for planned close-kin mark–recapture analyses. The low observed effective size also has conservation implications. Both issues warrant continued genetic monitoring.

Sibling competition, dispersal and fitness outcomes in humans

Determining how sibling interactions alter the fitness outcomes of dispersal is pivotal for the understanding of family living, but such studies are currently scarce. Using a large demographic dataset on pre-industrial humans from Finland, we studied dispersal consequences on different indicators of lifetime reproductive success according to sex-specific birth rank (a strong determinant of dispersal in our population). Contrary to the predictions of the leading hypotheses, we found no support for differential fitness benefits of dispersal for either males or females undergoing low vs. high sibling competition. Our results are inconsistent with both hypotheses that family members could have different fitness maximizing strategies depending on birth rank, and that dispersal could be mainly driven by indirect fitness benefits for philopatric family members. Our study stresses the need for studying the relative outcomes of dispersal at the family level in order to understand the evolution of family living and dispersal behaviour.

Climatic forcing and individual heterogeneity in a resident mountain bird: legacy data reveal effects on reproductive strategies.

Optimization of clutch size and timing of reproduction have substantial effects on lifetime reproductive success in vertebrates, and both individual quality and environmental variation may impact life history strategies. We tested hypotheses related to maternal investment and timing of reproduction, using 17 years (1978-1994) of individual-based life history data on willow ptarmigan (Lagopus l. lagopus, n = 290 breeding females with n = 319 breeding attempts) in central Norway. We analysed whether climatic variation and individual state variables (age and body mass) affected the number of offspring and timing of reproduction, and individual repeatability in strategies. The results suggest that willow ptarmigan share a common optimal clutch size that is largely independent of measured individual states. While we found no clear direct weather effects on clutch size, higher spring temperatures advanced onset of breeding, and early breeding was followed by an increased number of offspring. Warmer springs were positively related to maternal mass, and mass interacted with clutch size in production of hatchlings. Finally, clutch size and timing of reproduction were highly repeatable within individuals, indicating that individual quality guided trade-offs in reproductive effort. Our results demonstrate how climatic forcing and individual heterogeneity in combination influenced life history traits in a resident montane keystone species.

Drivers and consequences of female reproductive competition in an egalitarian, sexually monomorphic primate

Even after the 150th anniversary of sexual selection theory, the drivers and mechanisms of female sexual selection remain poorly studied. To understand demographic circumstances favoring female-female competition, trade-offs with kin selection and interactions with male reproductive strategies, we investigated female evictions in redfronted lemurs (Eulemur rufifrons). Based on 24 years of demographic data of known individuals, we show that female redfronted lemurs target close female kin for forcible, permanent, and presumably lethal eviction, even though groups contain multiple unrelated males whose voluntary emigration actually mitigated the probability of future female evictions. Female eviction and male emigration were predicted by group size, but male emigration was primarily driven by a proportional increase of male rivals. Female evictions were more likely than male emigrations when there were more juvenile females in a group, but the identity of evicted females was not predicted by any intrinsic traits. While birth rates were reduced by the number of juvenile females, they were higher when there were more adult females in a group and in years with more rainfall. Early infant survival was reduced with increasing numbers of juvenile females, but variation in female lifetime reproductive success was not related to any of the predictors examined here. Thus, there seems to be a limit on female group size in this lemur species. More generally, our study demonstrates a balanced interplay between female reproductive competition, competition over group membership between both sexes, and kin selection, contributing new insights into the causes and consequences of female competition in animal societies.Significance statementThe evolutionary causes of female competition in vertebrate societies remain poorly known. Evictions represent an extreme form of female competition because even close kin are evicted when same-sized unrelated males are theoretically also available as victims. We studied drivers and consequences of evictions in redfronted lemurs (Eulemur rufifrons) using 24 years of demographic data from multiple groups. We show that while voluntary male emigration mitigates the probability of future female evictions, females nonetheless appear to accept the fitness costs of evicting female kin. While group size seems to be the main driver of departures by either sex, the number of juvenile females present in groups is the key variable triggering eviction events as well as physiological responses that could be interpreted as female reproductive restraint. Our study therefore revealed that competition does trump cooperation under some circumstances in the intricate interplay between sexual selection and kin selection on females.

Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wild Drosophila melanogaster.

Strong sexual selection frequently leads to sexual conflict and ensuing male harm, whereby males increase their reproductive success at the expense of harming females. Male harm is a widespread evolutionary phenomenon with a strong bearing on population viability. Thus, understanding how it unfolds in the wild is a current priority. Here, we sampled a wild Drosophila melanogaster population and studied male harm across the normal range of temperatures under which it reproduces optimally in nature by comparing female lifetime reproductive success and underlying male harm mechanisms under monogamy (i.e. low male competition/harm) vs. polyandry (i.e. high male competition/harm). While females had equal lifetime reproductive success across temperatures under monogamy, polyandry resulted in a maximum decrease of female fitness at 24°C (35%), reducing its impact at both 20°C (22%), and 28°C (10%). Furthermore, female fitness components and pre- (i.e. harassment) and post-copulatory (i.e. ejaculate toxicity) mechanisms of male harm were asymmetrically affected by temperature. At 20°C, male harassment of females was reduced, and polyandry accelerated female actuarial aging. In contrast, the effect of mating on female receptivity (a component of ejaculate toxicity) was affected at 28°C, where the mating costs for females decreased and polyandry mostly resulted in accelerated reproductive aging. We thus show that, across a natural thermal range, sexual conflict processes and their effects on female fitness components are plastic and complex. As a result, the net effect of male harm on overall population viability is likely to be lower than previously surmised. We discuss how such plasticity may affect selection, adaptation and, ultimately, evolutionary rescue under a warming climate.

Null Models for the Opportunity for Selection.

AbstractCrow's "opportunity for selection" ( in relative fitness) is an important albeit controversial eco-evolutionary concept, particularly regarding the most appropriate null model(s). Here, we treat this topic in a comprehensive way by considering opportunities for both fertility selection (If) and viability selection (Im) for discrete generations, both seasonal and lifetime reproductive success in age-structured species, and experimental designs that include either a full or partial life cycle, with complete enumeration or random subsampling. For each scenario, a null model that includes random demographic stochasticity can be constructed that follows Crow's initial formulation that . The two components of I are qualitatively different. Whereas an adjusted If () can be computed that accounts for random demographic stochasticity in offspring number, Im cannot be similarly adjusted in the absence of data on phenotypic traits under viability selection. Including as potential parents some individuals that die before reproductive age produces an overall zero-inflated Poisson null model. It is always important to remember that (1) Crow's I represents only the opportunity for selection and not selection itself and (2) the species' biology can lead to random stochasticity in offspring number that is either overdispersed or underdispersed compared with the Poisson (Wright-Fisher) expectation.

Evaluating the evolutionary mechanisms maintaining alternative mating strategies in a simulated bull trout (Salvelinus confluentus) population.

The coexistence of distinct alternative mating strategies (AMS) is often explained by mechanisms involving trade-offs between reproductive traits and lifetime fitness; yet their relative importance remains poorly understood. Here, we used an established individual-based, spatially explicit model to simulate bull trout (Salvelinus confluentus) in the Skagit River (Washington, USA) and investigated the influence of female mating preference, sneaker-specific mortality, and variation in age-at-maturity on AMS persistence using global sensitivity analyses and boosted regression trees. We assumed that two genetically fixed AMS coexisted within the population: sneaker males (characterized by younger age-at-maturity, greater AMS-specific mortality, and lower reproductive fitness) and territorial males. After 300 years, variation in relative sneaker success in the system was explained by sneaker males' reproductive fitness (72%) and, to a lesser extent, the length of their reproductive lifespan (21%) and their proportion in the initial population (8%). However, under a wide range of parameter values, our simulated scenarios predicted the extinction of territorial males or their persistence in small, declining populations. Although these results do not resolve the coexistence of AMS in salmonids, they reinforce the importance of mechanisms reducing sneaker's lifetime reproductive success in favoring AMS coexistence within salmonid populations but also limit the prediction that, without any other selective mechanisms at play, strong female preference for mating with territorial males and differences in reproductive lifespan allow the stable coexistence of distinct AMS.

Reproductive success of jack and full-size males in a wild coho salmon population.

Despite the wealth of research on Pacific salmon Oncorhynchus spp. life histories there is limited understanding of the lifetime reproductive success of males that spend less time at sea and mature at a smaller size (jacks) than full-size males. Over half of returning male spawners can be jacks in some populations, so it is crucial to understand their contribution to population productivity. We quantified adult-to-adult reproductive success (RS) of jacks and their relative reproductive success (RRS) compared to full-size males in a wild population of coho salmon in the Auke Creek watershed, Juneau, Alaska. We used genetic data from nearly all individuals (approx. 8000) returning to spawn over a decade (2009-2019) to conduct parentage analysis and calculate individual RS. The average adult-to-adult RS of jacks (mean = 0.7 and s.e. = 0.1) was less than that of full-size males (mean = 1.1 and s.e. = 0.1). Jack RRS was consistently below 1.0 but ranged widely (0.23 to 0.96). Despite their lower average success, jacks contributed substantially to the population by siring 23% of the total returning adult offspring (1033 of 4456) produced between 2009 and 2015. Our results imply that jacks can affect evolutionary and population dynamics, and are relevant to the conservation and management of Pacific salmon.

Do females of Whiskered Tern Chlidonias hybrida renest after offspring desertion?

In species with biparental care, one parent may relieve him-/herself of the costs of parental care by deserting and leaving the mate to care for the offspring. Offspring desertion by a single parent, usually the female, occurs in many bird species, especially in Charadriiformes. The reasons for desertion are still being debated, and compelling evidence for the benefits and costs to either sex is not yet handed. The benefits of desertion for the deserter may include renesting with a new mate shortly after desertion. Therefore, desertion may enhance individual lifetime reproductive success. In Whiskered Tern Chlidonias hybrida almost all females desert, about half of females desert during chick-rearing period, the other half during the post-fledging period. Based on intensive fieldwork over a 4-year study, we investigated whether Whiskered Tern females remated and renested after desertion. We assumed that favourable conditions, such as an extended breeding season and food abundance resulting in a high breeding success would prompt most females to renest after desertion. In contrast to this expectation, however, only 5% of females that deserted during chick-rearing period (2 out of 41) remated and renested in the study area. About 50 days elapsed between the initiations of the first and second clutch by these two females. Females also participated in courtship behaviour after desertion (without renesting). We thus estimate that 15% (6 out of 41) of females that deserted during chick-rearing period were subsequently involved in some kind of breeding activity. Therefore, renesting does not seem to be a major direct benefit for deserting Whiskered Tern females. Females of this species probably benefit from desertion in other ways, but these have yet to be discovered.

Fit-Seq2.0: An Improved Software for High-Throughput Fitness Measurements Using Pooled Competition Assays

The fitness of a genotype is defined as its lifetime reproductive success, with fitness itself being a composite trait likely dependent on many underlying phenotypes. Measuring fitness is important for understanding how alteration of different cellular components affects a cell’s ability to reproduce. Here, we describe an improved approach, implemented in Python, for estimating fitness in high throughput via pooled competition assays.

Philopatry yields higher fitness than dispersal in a cooperative breeder with sex-specific life history trajectories.

Social evolution is tightly linked to dispersal decisions, but the ecological and social factors selecting for philopatry or dispersal often remain obscure. Elucidating selection mechanisms underlying alternative life histories requires measurement of fitness effects in the wild. We report on a long-term field study of 496 individually marked cooperatively breeding fish, showing that philopatry is beneficial as it increases breeding tenure and lifetime reproductive success in both sexes. Dispersers predominantly join established groups and end up in smaller groups when they ascend to dominance. Life history trajectories are sex specific, with males growing faster, dying earlier, and dispersing more, whereas females more likely inherit a breeding position. Increased male dispersal does not seem to reflect an adaptive preference but rather sex-specific differences in intrasexual competition. Cooperative groups may thus be maintained because of inherent benefits of philopatry, of which females seem to get the greater share in social cichlids.

Why do parents produce small broods of offspring that have lower body mass, survival, and lifetime reproductive success? A case study in a long-lived bird

Why do parents produce small broods of offspring that have lower body mass, survival, and lifetime reproductive success? A case study in a long-lived bird

Modeling of senescent cell dynamics predicts a late-life decrease in cancer incidence.

Current oncogenic theories state that tumors arise from cell lineages that sequentially accumulate (epi)mutations, progressively turning healthy cells into carcinogenic ones. While those models found some empirical support, they are little predictive of intraspecies age-specific cancer incidence and of interspecies cancer prevalence. Notably, in humans and lab rodents, a deceleration (and sometimes decline) of cancer incidence rate has been found at old ages. Additionally, dominant theoretical models of oncogenesis predict that cancer risk should increase in large and/or long-lived species, which is not supported by empirical data. Here, we explore the hypothesis that cellular senescence could explain those incongruent empirical patterns. More precisely, we hypothesize that there is a trade-off between dying of cancer and of (other) ageing-related causes. This trade-off between organismal mortality components would be mediated, at the cellular scale, by the accumulation of senescent cells. In this framework, damaged cells can either undergo apoptosis or enter senescence. Apoptotic cells lead to compensatory proliferation, associated with an excess risk of cancer, whereas senescent cell accumulation leads to ageing-related mortality. To test our framework, we build a deterministic model that first describes how cells get damaged, undergo apoptosis, or enter senescence. We then translate those cellular dynamics into a compound organismal survival metric also integrating life-history traits. We address four different questions linked to our framework: can cellular senescence be adaptive, do the predictions of our model reflect epidemiological patterns observed among mammal species, what is the effect of species sizes on those answers, and what happens when senescent cells are removed? Importantly, we find that cellular senescence can optimize lifetime reproductive success. Moreover, we find that life-history traits play an important role in shaping the cellular trade-offs. Overall, we demonstrate that integrating cellular biology knowledge with eco-evolutionary principles is crucial to solve parts of the cancer puzzle.

Evidence of an Absence of Inbreeding Depression in a Wild Population of Weddell Seals (Leptonychotes weddellii).

Inbreeding depression can reduce the viability of wild populations. Detecting inbreeding depression in the wild is difficult; developing accurate estimates of inbreeding can be time and labor intensive. In this study, we used a two-step modeling procedure to incorporate uncertainty inherent in estimating individual inbreeding coefficients from multilocus genotypes into estimates of inbreeding depression in a population of Weddell seals (Leptonychotes weddellii). The two-step modeling procedure presented in this paper provides a method for estimating the magnitude of a known source of error, which is assumed absent in classic regression models, and incorporating this error into inferences about inbreeding depression. The method is essentially an errors-in-variables regression with non-normal errors in both the dependent and independent variables. These models, therefore, allow for a better evaluation of the uncertainty surrounding the biological importance of inbreeding depression in non-pedigreed wild populations. For this study we genotyped 154 adult female seals from the population in Erebus Bay, Antarctica, at 29 microsatellite loci, 12 of which are novel. We used a statistical evidence approach to inference rather than hypothesis testing because the discovery of both low and high levels of inbreeding are of scientific interest. We found evidence for an absence of inbreeding depression in lifetime reproductive success, adult survival, age at maturity, and the reproductive interval of female seals in this population.

Oviposition experience promotes active reproductive behaviour in a synovigenic parasitoid

Parasitoids are important insects that are commonly released into the environment to reduce the population sizes of pest species. The lifetime reproductive success of parasitoids mainly depends on host availability and the availability of mature eggs. Consequently, it is predicted that female wasps must balance the risk of egg or host (time) limitation with maximized lifetime fecundity. Typically, synovigenic females, which continue to mature eggs throughout their lifetime, have been shown to adjust their egg production rate in response to environmental variations in host availability to reduce the risk of egg limitation. In this study, we found that in a synovigenic egg parasitoid, Anastatus japonicus (Hymenoptera: Eupelmidae), the oviposition experience of Ana. japonicus females significantly enhanced the egg load and increased the rate of mature egg production. However, in contrast to other studies, the experience of contact with a host did not significantly affect the egg load in females. This result suggests that the overall oviposition experience might induce an adjustment and accelerate egg maturation in Ana. japonicus and is likely more important in egg maturation than transitory host contract. In addition to affecting the egg load, oviposition experience influenced Ana. japonicus female reproductive behaviour, which shifted virgin female behavioural preferences from mating to oviposition and laying more eggs per clutch. Our study provides an optimal strategy for the post-oviposition release of Ana. japonicus, an egg parasitoid of several lepidopteran forest pests, to improve biocontrol effectiveness.

Genomic signatures of inbreeding depression for a threatened Aotearoa New Zealand passerine.

For small and isolated populations, the increased chance of mating between related individuals can result in a substantial reduction in individual and population fitness. Despite the increasing availability of genomic data to measure inbreeding accurately across the genome, inbreeding depression studies for threatened species are still scarce due to the difficulty of measuring fitness in the wild. Here, we investigate inbreeding and inbreeding depression for the extensively monitored Tiritiri Mātangi island population of a threatened Aotearoa New Zealand passerine, the hihi (Notiomystis cincta). First, using a custom 45 k single nucleotide polymorphism (SNP) array, we explore genomic inbreeding patterns by inferring homozygous segments across the genome. Although all individuals have similar levels of ancient inbreeding, highly inbred individuals are affected by recent inbreeding, which can probably be explained by bottleneck effects such as habitat loss after European arrival and their translocation to the island in the 1990s. Second, we investigate genomic inbreeding effects on fitness, measured as lifetime reproductive success, and its three components, juvenile survival, adult annual survival and annual reproductive success, in 363 hihi. We find that global inbreeding significantly affects juvenile survival but none of the remaining fitness traits. Finally, we employ a genome-wide association approach to test the locus-specific effects of inbreeding on fitness, and identify 13 SNPs significantly associated with lifetime reproductive success. Our findings suggest that inbreeding depression does impact hihi, but at different genomic scales for different traits, and that purging has therefore failed to remove all variants with deleterious effects from this population of conservation concern.