Lower Lifetime Reproductive Success Research Articles

Sexual selection buffers the negative consequences of population fragmentation on adaptive plastic responses to increasing temperatures.

Whether sexual selection facilitates or hampers the ability to plastically respond to novel environments might depend on population structure, via its effects on sexual interactions and associated fitness payoffs. Using experimentally evolved lines of the seed beetle Callosobruchus maculatus, we tested whether individuals evolving under different sexual selection (monogamy vs. polygamy) and population spatial structure (metapopulation vs. undivided populations) treatments differed in their response across developmental thermal conditions (control, hot, or stressful) in a range of fitness and fitness-associated traits. We found that individuals from subdivided populations had lower lifetime reproductive success at hot temperatures, but only in lines evolving under relaxed sexual selection, revealing a complex interaction between sexual selection, population structure, and thermal environmental stress on fitness. We also found an effect of population structure on several traits, including fertility and adult emergence success, under exposure to high thermal conditions. Finally, we found a strong negative effect of hot and stressful temperatures on fitness and associated traits. Our results show that population structure can exacerbate the impact of a warming climate, potentially leading to declines in population viability, but that sexual selection can buffer the negative influence of population subdivision on adaptation to warm temperatures.

The Feast and the Famine: Spring Body Mass Variations and Life History Traits in a Pulse Resource Ecosystem.

AbstractPhenotypic plasticity is the most immediate mechanism of adaptative response to environmental change. Studying plastic changes in response to fluctuating environments provides insights into how such adjustments may impact life history traits. Here, we used a 14-year data set of repeated body mass measurements in male eastern chipmunks (Tamias striatus) to assess the extent of plastic changes for this trait in a resource pulse ecosystem. We first determined the magnitude of variation in body mass at the population level in response to the drastic change in food resource availability from American beech tree seeds (Fagus grandifolia). Males that emerged in the spring from winter torpor following a nonmast year had a lower body mass than males emerging after a mast year, but they tended to recover this loss by mid-June. We found significant among-individual variation in spring body mass plasticity (i.e., individual-by-environment interaction). We then investigated the relationships between individual spring body mass plasticity, longevity, and lifetime reproductive success. Interestingly, heavier males lived longer than lighter males, but more plastic males had a lower longevity and lower lifetime reproductive success than less plastic males. The report of such plastic response in a stochastic resource system provides valuable insights into the interplay between the costs and benefits of phenotypic plasticity as an adaptation to environmental fluctuations.

Staging to join non-kin groups in a classical cooperative breeder, the Florida scrub-jay.

Why unrelated members form groups in animal societies remains a pertinent topic in evolutionary biology because benefits for group members often are not obvious. We studied subordinates that disperse to join unrelated social groups in the Florida scrub-jay Aphelocoma coerulescens, a cooperative breeding species mainly composed of kin-based groups. We evaluated potential adaptive benefits of dispersing to become an unrelated helper (staging) versus remaining home and dispersing only to pair and breed (direct dispersal) to understand why non-kin-based groups form. Using 35years of demographic data, we quantified life-history aspects of staging individuals and tested associations between social and ecological factors on the natal and staging territories. We compared fitness outcomes between dispersal strategies by analysing survival, breeding recruitment and direct reproductive output. We tested for sexual asymmetry potentially driven by differences in territory acquisition patterns and female-biased dispersal for this species. Of birds that reached 1year, 28% staged at a non-natal territory before breeding or disappearing. Staging dispersers departed at younger ages and moved greater distances than direct dispersers. When looking at proximate factors on the natal territory associated with staging, males left groups with many same-sex helpers, while females often left when their father disappeared. For both sexes, staging individuals more likely came from high-quality territories and joined groups with fewer same-sex helpers than in their natal group. While staging and direct dispersers did not differ in survival or likelihood of becoming a breeder, staging males became breeders later and had lower lifetime reproductive success than direct dispersers. In Florida scrub-jays, staging appears to be an alternative strategy for female helpers, but a best-of-a-bad-situation for males. This sexual asymmetry is consistent with males having more options than females to achieve higher reproductive success by breeding near home. Trade-offs in cost-benefits of departing the natal territory and joining unrelated groups as a helper seem to best explain alternative dispersal patterns, with optimal social queues primarily driving the benefits. This research highlights plasticity in dispersal behaviour in response to social and environmental conditions and offers a new perspective in our understanding of non-kin-based social groups.

Impacts of a biocontrol agent on invasive Ageratina adenophora in Southwest China: Friend or foe?

Classical biological control of invasive plants depends on the introduction of host-specific natural enemies. Many natural enemies have provided successful control, but the impacts of herbivorous insects on their hosts are highly variable and context dependent. Under some circumstances, overcompensation can even occur, with plant reproduction temporarily increasing rather than decreasing in response to herbivory. The stem-galling fly Procecidochares utilis has been widely introduced to help control Ageratina adenophora, a globally significant weed, but its impact has been inconsistent and in places ineffective. Its galling is known to stimulate production of side branches in plants under laboratory conditions. We examined the abundance and impact of P. utilis at four A. adenophora sites of Southwest China that were invaded at different times and support different densities of the insect. Stems with galls were more likely to be branched and produced more capitula. Furthermore, seed numbers in capitula from galled and un-galled stems were similar, and galling resulted in only slightly reduced seed weights. However, the increase in above-ground vegetative biomass associated with branching resulted in less efficient capitulum production relative to vegetative growth. Clearly Procecidochares utilis is not providing effective biocontrol of Ageratina adenophora in Southwest China so far. In the long term, galled plants may display reduced competitive ability and lower lifetime reproductive success, but the short term increases in seed production it generates suggest it may be favouring its host’s range expansion. The fly has been a successful biocontrol agent in dry area of Hawii, so understanding the factors that determine its effectiveness represent a major challenge for the future.

Juvenile rank acquisition is associated with fitness independent of adult rank.

Social rank is a significant determinant of fitness in a variety of species. The importance of social rank suggests that the process by which juveniles come to establish their position in the social hierarchy is a critical component of development. Here, we use the highly predictable process of rank acquisition in spotted hyenas to study the consequences of variation in rank acquisition in early life. In spotted hyenas, rank is 'inherited' through a learning process called 'maternal rank inheritance.' This pattern is very consistent: approximately 80% of juveniles acquire the exact rank expected under the rules of maternal rank inheritance. The predictable nature of rank acquisition in these societies allows the process of rank acquisition to be studied independently from the ultimate rank that each juvenile attains. In this study, we use Elo-deviance scores, a novel application of the Elo-rating method, to calculate each juvenile's deviation from the expected pattern of maternal rank inheritance during development. Despite variability in rank acquisition among juveniles, most of these juveniles come to attain the exact rank expected of them according to the rules of maternal rank inheritance. Nevertheless, we find that transient variation in rank acquisition in early life is associated with long-term fitness consequences for these individuals: juveniles 'underperforming' their expected ranks show reduced survival and lower lifetime reproductive success than better-performing peers, and this relationship is independent of both maternal rank and rank achieved in adulthood. We also find that multiple sources of early life adversity have cumulative, but not compounding, effects on fitness. Future work is needed to determine if variation in rank acquisition directly affects fitness, or if some other variable, such as maternal investment or juvenile condition, causes variation in both of these outcomes.

Lifetime reproductive success of northern elephant seals (Mirounga angustirostris)

Lifetime reproductive success of individuals in a natural population provides an estimate of Darwinian fitness. We calculated lifetime reproductive success in a colony of female northern elephant seals (Mirounga angustirostris (Gill, 1866)) by monitoring annual breeding throughout life of 7735 female weanlings marked individually at Año Nuevo, California, USA, from 1963 to 2005. Great variation in lifetime reproductive success was evident in three aspects of life history: (1) 75% of the females died before reaching breeding age and produced no pups; (2) nearly half of the survivors bred for only a few years before dying, and young females had low weaning success; (3) less than 1% of the females in the sample were exceptionally successful producing up to 20 pups in life. Many females that bred early, while still growing, had decreased lifespan, low weaning success, and lower lifetime reproductive success than females that postponed first breeding. Exceptional reproductive success was associated with giving birth annually, living long (up to age 23), and weaning large pups that were more likely to survive and breed. We conclude that there is strong selection for increased lifespan and multiparous supermoms that contribute significantly to pup production in the next generation.

Endoparasite infection has both short- and long-term negative effects on reproductive success of female house sparrows, as revealed by faecal parasitic egg counts.

Parasites have the potential to severely reduce host reproductive success. However, the effects of endoparasites on reproductive success have not received the same amount of attention as the effects of parasites on host survival. We investigated the relationship between an avian endoparasite (gapeworm, Syngamus trachea) and both current and future reproductive success of female house sparrows (Passer domesticus) in a population on the coast of Helgeland, northern Norway. We found that the proportion of eggs in a nest that failed to develop into fledglings increased as the faecal parasitic egg count of the mothers increased. We also found that juvenile females with high numbers of parasitic eggs in their faeces had lower lifetime reproductive success as adults. However, we did not find a relationship between maternal parasite infection and clutch size or recruitment rate of offspring. To our knowledge this is the first study to find a relationship between reproductive success of an avian host and faecal egg count of an endoparasite. The present study indicates that infection by an endoparasite may be associated with lower individual reproductive success in both the short-term and long-term in a wild population of hosts.

Are There Indirect Fitness Benefits of Female Extra-Pair Reproduction? Lifetime Reproductive Success of Within-Pair and Extra-Pair Offspring

The forces driving extra-pair reproduction by socially monogamous females, and the resulting genetic polyandry, remain unclear. A testable prediction of the hypothesis that extra-pair reproduction partly reflects indirect selection on females is that extra-pair young (EPY) will be fitter than their within-pair young (WPY) maternal half-siblings. This prediction has not been comprehensively tested in a wild population, requiring data on the lifetime reproductive success (LRS) of maternal half-sib EPY and WPY. We used 17 years of genetic parentage data from song sparrows, Melospiza melodia, to compare the LRS of hatched EPY and WPY maternal half-siblings measured as their lifetime number of hatched offspring, recruited offspring, and hatched grandoffspring. EPY hatchlings were not significantly fitter than WPY hatchlings for any of three measures of LRS. Furthermore, opposite to prediction, EPY hatchlings tended to have lower LRS than their maternal half-sibling WPY hatchlings on average. EPY also tended to be less likely to survive to hatch than their maternal half-sibling WPY. Taken together, these results fail to support one key hypothesis explaining the evolution of genetic polyandry by socially monogamous females and suggest there may be weak indirect selection against female extra-pair reproduction in song sparrows.

Individual variation in rates of senescence: natal origin effects and disposable soma in a wild bird population

1. Longitudinal studies of various vertebrate populations have recently demonstrated senescent declines in reproductive performance and/or survival probability with age to be almost ubiquitous in nature. Little is known, however, about the extent to which rates of senescence vary between individuals, and about causes or consequences of such variation. Quantifying these links in natural populations is important for understanding the constraints and adaptive processes underlying the evolution of senescence. 2. Here, we analyse breeding data from 1029 female great tits Parus major to quantify the effect of natal conditions and early life reproduction on rates of reproductive senescence, reproductive life span and lifetime reproductive success. 3. Although for locally born females we find no evidence that natal conditions influence rates of reproductive senescence, we show that immigrant females suffer from faster rates of senescence than locally born females, and that this difference contributes to immigrants having a lower lifetime reproductive success. 4. Additionally, and independently, we find rates of reproductive senescence to increase with rates of early life reproduction, as predicted by the disposable soma hypothesis. Despite accelerated senescence late in life, high early life reproduction is, however, positively associated with lifetime reproductive success across individuals. 5. Female immigrant status and early life reproduction do not relate to reproductive life span. 6. We thus show that both immigration into our population, and high levels of early life reproduction, are associated with reduced late life reproductive performance in female great tits, but that fitness can be increased by high levels of early life reproduction at the expense of accelerated reproductive senescence. These results suggest disposable soma to be a likely mechanism underlying senescence in these birds, and encourage further study of the genetic basis (i.e. antagonistic pleiotropy) of such an early vs. late life trade-off.

LIFE HISTORY CORRELATES OF ALTERNATIVE MIGRATORY STRATEGIES IN AMERICAN DIPPERS

Partial migration is thought to be a critical step in the evolution of avian migration, but data on the life history correlates of alternative migratory strategies are extremely limited. We have studied a partially migratory population of American Dippers since 1999. This population is composed of sedentary individuals (residents) that maintain the same territory year round and altitudinal migrants that share winter grounds with residents, but move to higher elevations to breed. We used seven years of data on individually marked birds to (1) determine if individuals consistently use the same migratory strategy, (2) determine if offspring have the same strategy as their parents, and (3) estimate reproductive and survival rates of the two migratory strategies. We evaluate hypotheses for the persistence of partial migration and discuss their implication for the evolution of migration in sedentary populations. Individual American Dippers rarely switched migratory strategy (4/169 monitored more than one year). An individual's strategy, however, was not always that of its parents, indicating that, while migratory behavior may have a genetic component, environmental or social conditions probably influence the migratory strategy that an individual adopts. Sedentary dippers consistently had higher annual productivity (approximately 1.4 more fledglings/year) than migratory dippers, but mark-recapture models suggested that migratory dippers may have slightly higher survival than residents (approximately 3.4%). Migrants were estimated to have lower lifetime reproductive success than residents because their higher survival was insufficient to offset their lower productivity. Our data suggest that alternative migratory strategies in American Dippers are unlikely to be a fixed genetic dimorphism that persists because the two strategies have equal fitness, or because the relative fitness of the two strategies fluctuates over time. Migratory strategies in American Dippers are more likely to be condition dependent, and the two strategies persist because migrants "make the best of a bad job" by moving to higher elevations to breed. Because migrants obtained no fitness benefits by moving to seasonal breeding territories, our data are consistent with the hypothesis that migration could evolve in sedentary populations if competition for limited resources forces some individuals to seek breeding opportunities outside their initial range.

LIFETIME AND INTERGENERATIONAL FITNESS CONSEQUENCES OF HARMFUL MALE INTERACTIONS FOR FEMALE LIZARDS

Male mating behaviors harmful to females have been described in a wide range of species. However, the direct and indirect fitness consequences of harmful male behaviors have been rarely quantified for females and their offspring, especially for long-lived organisms under natural conditions. Here, lifetime and intergenerational consequences of harmful male interactions were investigated in female common lizards (Lacerta vivipara) using field experiments. We exposed females to male harm by changing the population sex ratio from a normal female-biased to an experimental male-biased sex ratio during the first experimental year. Thereafter, females and their first generation of offspring were monitored during two additional years in a common garden with a female-biased sex ratio. We found strong immediate fitness costs and lower lifetime reproductive success in females subjected to increased male exposure. The immediate fitness costs were partly mitigated by direct compensatory responses after exposure to male excess, but not by indirect benefits through offspring growth, offspring survival, or mating success of offspring. These results support recent empirical findings showing that the direct costs of mating are not outweighed by indirect benefits.

Mating Frequency and Inclusive Fitness in Drosophila melanogaster

In many species, increased mating frequency reduces maternal survival and reproduction. In order to understand the evolution of mating frequency, we need to determine the consequences of increased mating frequency for offspring. We conducted an experiment in Drosophila melanogaster in which we manipulated the mating frequency of mothers and examined the survival and fecundity of the mothers and their daughters. We found that mothers with the highest mating frequency had accelerated mortality and more rapid reproductive senescence. On average, they had 50% shorter lives and 30% lower lifetime reproductive success (LRS) than did mothers with the lowest mating frequency. However, mothers with the highest mating frequency produced daughters with 28% greater LRS. This finding implies that frequent mating stimulates cross-generational fitness trade-offs such that maternal fitness is reduced while offspring fitness is enhanced. We evaluate these results using a demographic metric of inclusive fitness. We show that the costs and benefits of mating frequency depend on the growth rate of the population. In an inclusive fitness context, there was no evidence that increased mating frequency results in fitness costs for mothers. These results indicate that cross-generational fitness trade-offs have an important role in sexual selection and life-history evolution.

Delayed Breeding Affects Lifetime Reproductive Success Differently in Male and Female Green Woodhoopoes

In cooperatively breeding species, many individuals only start breeding long after reaching physiological maturity [1], and this delay is expected to reduce lifetime reproductive success (LRS) [1-3]. Although many studies have investigated how nonbreeding helpers might mitigate the assumed cost of delayed breeding (reviewed in [3]), few have directly quantified the cost itself [4, 5] (but see [6, 7]). Moreover, although life-history tradeoffs frequently influence the sexes in profoundly different ways [8, 9], it has been generally assumed that males and females are similarly affected by a delayed start to breeding [7]. Here, we use 24 years of data to investigate the sex-specific cost of delayed breeding in the cooperatively breeding green woodhoopoe (Phoeniculus purpureus) and show that age at first breeding is related to LRS differently in males and females. As is traditionally expected, males that started to breed earlier in life had greater LRS than those that started later. However, females showed the opposite pattern: Those individuals that started to breed later in life actually had greater LRS than those that started earlier. In both sexes, the association between age at first breeding and LRS was driven by differences in breeding-career length, rather than per-season productivity. We hypothesize that the high mortality rate of young female breeders, and thus their short breeding careers, is related to a reduced ability to deal with the high physiological costs of reproduction in this species. These results demonstrate the importance of considering sex-specific reproductive costs when estimating the payoffs of life-history decisions and bring into question the long-held assumption that delayed breeding is necessarily costly.

Age at first breeding and fitness in goshawk Accipiter gentilis

Summary Age at first breeding has a large influence on fitness and hence is crucial to the evolution of life‐history strategies. Goshawks Accipiter gentilis start breeding aged 1–4 years. Using 30 years of data and both lifetime reproductive success (LRS) and lind as a fitness estimate for 74 female goshawks, I showed that the optimal age at first reproduction was 3 years in this population. Females that started to breed earlier had lower LRS and lind, not because of reduced life span, but because of lower reproduction at early ages. The constraint hypothesis, which states that foraging or other skills improve with age was the most likely explanation for the higher reproduction with increasing age. Incorporating habitat heterogeneity provided the mechanism that explained not only the fitness cost to early maturity, but also why this cost was heterogeneous. Females starting to breed aged 1 suffered a very high fitness cost if they were in a bad‐quality territory, but fitness costs were small when they were in a good‐quality territory. This explains why I found evidence for a nonlinear selection pressure on age at first breeding. Population density also affected whether a female started to breed early or not: over the study period, population density increased and the percentage of females starting to breed aged 1 decreased. The optimal age at first breeding seems to be a trait affected by a complex interplay between cost and benefits of early reproduction mediated by habitat heterogeneity and population density.