Life-history plasticity and inbreeding depression under mate limitation and predation risk: cumulative lifetime fitness dissected with a life table response experiment

Environmental effects on the evolution of mating systems are increasingly discussed, but we lack many examples of how environmental conditions affect the expression and consequences of alternative mating systems. Variation in mate availability sets up a trade-off between reproductive assurance and inbreeding depression, but the consequences of both mate limitation and inbreeding may depend on other environmental conditions. Predation risk is common under natural conditions, and known to affect allocation to reproduction, but we know little about the effects of isolation and inbreeding under predation risk. We reared selfed and outcrossed hermaphroditic freshwater snails (Physa acuta) in four environments (predator cues present or absent crossed with mating partners available or not) and quantified life-history traits and cumulative lifetime fitness. Our results confirm that isolation from mates can increase longevity and growth, resulting in higher lifetime fecundity. Thus, we observed no evidence for mate limitation of reproduction. However, reproduction under isolation (i.e., selfing) resulted in inbreeding depression, which should counteract the benefits of selfing. Inbreeding depression in fitness occurred in both predator and no-predator environments, but there was no overall change in inbreeding depression with predator cues. This represents, to our knowledge, the first empirical estimate of the effect of predation risk on inbreeding depression in an animal. Cumulative fitness was most influenced by early survival and especially early fecundity. As predation risk and inbreeding (both ancestral and due to a lack of mates) reduced early fecundity, these effect are predicted to have important contributions to population growth under natural conditions. Therefore life-history plasticity (e.g., delayed reproduction) is likely to be very important to overall fitness.     

Primates and the evolution of long, slow life histories

Primates are characterized by relatively late ages at first reproduction, long lives and low fertility. Together, these traits define a life-history of reduced reproductive effort. Understanding the optimal allocation of reproductive effort, and specifically reduced reproductive effort, has been one of the key problems motivating the development of life-history theory. Because of their unusual constellation of life-history traits, primates play an important role in the continued development of life-history theory. In this review, I present the evidence for the reduced reproductive effort life histories of primates and discuss the ways that such life-history tactics are understood in contemporary theory. Such tactics are particularly consistent with the predictions of stochastic demographic models, suggesting a key role for environmental variability in the evolution of primate life histories. The tendency for?primates to specialize in high-quality, high-variability food items may make them particularly susceptible to environmental variability and explains their?low reproductive-effort tactics. I discuss recent applications of life-history theory to human evolution and emphasize the continuity between models used to explain peculiarities of human reproduction and senescence with the long, slow life histories of primates more generally.     

Does Predation Risk Affect Mating Behavior? An Experimental Test in Dumpling Squid (Euprymna tasmanica)

Introduction

One of the most important trade-offs for many animals is that between survival and reproduction. This is particularly apparent when mating increases the risk of predation, either by increasing conspicuousness, reducing mobility or inhibiting an individual''s ability to detect predators. Individuals may mitigate the risk of predation by altering their reproductive behavior (e.g. increasing anti-predator responses to reduce conspicuousness). The degree to which individuals modulate their reproductive behavior in relation to predation risk is difficult to predict because both the optimal investment in current and future reproduction (due to life-history strategies) and level of predation risk may differ between the sexes and among species. Here, we investigate the effect of increased predation risk on the reproductive behavior of dumpling squid (Euprymna tasmanica).

Results

Females, but not males, showed a substantial increase in the number of inks (an anti-predator behavior) before mating commenced in the presence of a predator (sand flathead Platycephalus bassensis). However, predation risk did not affect copulation duration, the likelihood of mating, female anti-predator behavior during or after mating or male anti-predator behavior at any time.

Conclusions

Inking is a common anti-predator defense in cephalopods, thought to act like a smokescreen, decoy or distraction. Female dumpling squid are probably using this form of defense in response to the increase in predation risk prior to mating. Conversely, males were undeterred by the increase in predation risk. A lack of change in these variables may occur if the benefit of completing mating outweighs the risk of predation. Prioritizing current reproduction, even under predation risk, can occur when the chance of future reproduction is low, there is substantial energetic investment into mating, or the potential fitness payoffs of mating are high.     

Parasite-induced risk of mortality elevates reproductive effort in male Drosophila.

A trade-off between sex and somatic maintenance is fundamental to life-history theory. Tests of this trade-off usually emphasize deleterious consequences of increased reproduction on life span. Here we show the reverse effect, that reductions in the expected life span elevate sexual activity. Experimentally parasitized male Drosophila nigrospiracula lived shorter lives, but before dying, they courted females significantly more than unparasitized controls. This greater courtship resulted in increased mating speed, and potentially greater reproductive success than parasitized males would have achieved otherwise. The results show that an environmental reduction in life span increases reproductive effort, and support the hypothesis of a trade-off between these key life-history traits.     

Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity

One of the most studied life-history trade-offs is that resulting from the cost of reproduction: a trade-off arises when reproduction diverts limited resources from other life-history traits. We examine the cost of reproduction in male, and the effect of male mating status on female Callosobruchus maculatus seed beetles. Cost of reproduction for male C. maculatus was manifested as reduced longevity. There was also a positive relationship between male body size and male longevity. Females mated to males that had already copulated twice did not live as long as females mated to males that had copulated once or not at all. The third copulation of males also lasted longer than the two previous ones. We conclude that even though the cost of reproduction for males has been studied much less than that in females, there is growing evidence that male reproductive effort is more complex than has traditionally been thought.     

Delayed selfing and resource reallocations in relation to mate availability in the freshwater snail Physa acuta

We study the influence of mate availability on the mating behavior of the self-fertile, preferentially outcrossing freshwater snail Physa acuta. Previous optimization theory indicated that mating system interacts with life-history traits to influence the age at first reproduction, providing three testable predictions. First, isolated individuals should reproduce later than individuals with available mates in the expectancy of finding a partner and avoiding the cost of inbreeding. Second, resource reallocation to future fecundity is needed for such reproductive delays to evolve. Third, the reproductive delay can be optimized with respect to life-history traits (e.g., survival, growth) and the mating system (inbreeding depression). Our results largely validate these predictions. First, reproduction is significantly delayed in isolated individuals ("selfers") as compared with individuals frequently exposed to mates ("outcrossers"). Second, delayed reproduction is associated with reallocation to future growth, survival, and fecundity, although fecundity is also affected by the mating system (selfing vs. outcrossing). Third, the reproductive delay found (approximately 2 wk) is consistent with quantitative predictions from optimization models. The delay is largely heritable, which might be partly explained by among-family differences in the amount of inbreeding depression (mating system) but not growth or survival.     

Hormonal responses differ when playing violent video games against an ingroup and outgroup

For 14 teams of three young men, salivary testosterone and cortisol were assessed twice before and twice after competing in within-group and between-group video games that simulated violent male–male competition. Men who contributed the most to their teams' between-group victory showed testosterone increases immediately after the competition, but only if this competition was played before the within-group tournament. High-scoring men on losing teams did not show this immediate effect, but they did show a delayed increase in testosterone. In contrast, high-ranking men tended to have lower testosterone and higher cortisol during within-group tournaments. The results are consistent with the hypothesis that men's competitive testosterone response varies across ingroup and outgroup competitions and is muted during the former. The testosterone response during the between-group competition also suggests that violent multiplayer video games may be appealing to young men because they simulate male–male coalitional competition.     

Adult Responses to Larval Population Size in the Almond Moth, Cadra cautella

Juvenile population size may affect the potential for future mating opportunities and therefore potentially sperm competition; this may favour ontogenetic adjustments in sperm production. Theory predicts that males should optimize their ejaculatory investment in accordance with the risk of sperm competition. Evidence for these theories is typically revealed in males of highly polyandrous species. Whether such responses to environmental cues exist for females, or are maintained in mildly polyandrous species in which most females do not re-mate, is unknown. Male lepidopterans produce normal, fertilizing sperm (eupyrene) and non-fertilizing (apyrene) sperm. Apyrene sperm are associated with reduced female receptivity, suggesting a role in sperm competition. We tested the effect of juvenile population size on life-history parameters and reproductive investment in the mildly polyandrous almond moth, Cadra cautella , a species in which current male ejaculate traits suggest previous selection for paternity protection consistent with a sperm-competitive environment. Larvae were reared at high (H) or low population sizes (L). We recorded larval development time, adult longevity and male gametic investment. Our results show a response by adults to signals in the juvenile environment. H males transferred more apyrene, but not eupyrene sperm. We also examined potential trade-offs between somatic characters and reproductive behaviours. Larval duration was longer for H individuals, females and heavier individuals. Further, H females and L males lived longer than L females. Our data are consistent with the theory that males should adjust their reproductive investment in accordance with sperm competition risk.     

Breeding frequency in Grey-headed Albatrosses Thalassarche chrysostoma

Although Grey-headed Albatrosses Thalassarche chrysostoma are usually regarded as biennial breeders, taking a year off following a successful breeding attempt, a small proportion of successful birds attempt to breed annually. This proportion was higher at Marion Island (5.4%) than at Bird Island, South Georgia (1.0%), suggesting that conditions are more favourable at Marion Island. This hypothesis is supported by higher average breeding success and shorter lags following both successful and failed breeding attempts at Marion Island. Factors favouring reproduction at Marion Island may include reduced intraspecific competition (given the much smaller breeding population) and/or more predictable food supply (owing to production of meso-scale eddies associated with the Indian Ocean Ridge). Although annual breeding appeared to increase the risk of adult mortality, with several birds that attempted to breed annually found dead the following year, at least some birds greatly enhanced their reproductive output, with one male raising five chicks in five successive years. Contrary to life-history theory, there was no evidence that older birds were more likely to attempt annual breeding because of declining reproductive value.     

Mating Behavior of Daphnia: Impacts of Predation Risk,Food Quantity,and Reproductive Phase of Females

High predation risk and food depletion lead to sexual reproduction in cyclically parthenogenetic Daphnia. Mating, the core of sexual reproduction, also occurs under these conditions. Assessment of the environmental conditions and alteration of mating efforts may aid in determining the success of sexual reproduction. Here, we evaluated the impacts of predation risk, food quantity, and reproductive phase of females on the mating behavior of Daphnia obtusa males including contact frequency and duration using video analysis. Mating–related behavior involved male–female contact (mating) as well as male–male contact (fighting). Mating frequency increased while unnecessary fighting decreased in the presence of predation risk. In addition, low food concentration reduced fighting between males. Males attempted to attach to sexual females more than asexual females, and fighting occurred more frequently in the presence of sexual females. Duration of mating was relatively long; however, males separated shortly after contact in terms of fighting behavior. Thus, assessment of environmental factors and primary sexing of mates were performed before actual contact, possibly mechanically, and precise sex discrimination was conducted after contact. These results suggest that mating in Daphnia is not a random process but rather a balance between predation risk and energetic cost that results in changes in mating and fighting strategies.     

三种同域分布喉毛花的繁殖分配

以青藏高原高寒草甸中三种同域分布的喉毛花为研究对象,通过比较三个种的植株性状和繁殖分配,探讨繁殖分配的种间差异及其与植株个体大小的关系。结果表明:(1)三个种的植株高度、顶花大小和单株花数目、繁殖分配均存在种间差异,这可能与其各自的交配系统和具体的生境以及相应的生活史对策有关;(2)在三种喉毛花中,投入到营养器官和繁殖器官的绝对资源量均呈显著正相关,未检测到植株生长和繁殖间的权衡关系;(3)三个种的个体大小与繁殖器官生物量均呈显著正相关,而与繁殖分配均呈显著负相关,这表明个体越大,繁殖投入越高,而繁殖分配越低,与以往研究结果一致,这可能是由于繁殖分配与个体大小之间存在异速关系。     

Reproductive sharing in relation to group and colony-level attributes in a cooperative breeding fish

The degree to which group members share reproduction is dictated by both within-group (e.g. group size and composition) and between-group (e.g. density and position of neighbours) characteristics. While many studies have investigated reproductive patterns within social groups, few have simultaneously explored how within-group and between-group social structure influence these patterns. Here, we investigated how group size and composition, along with territory density and location within the colony, influenced parentage in 36 wild groups of a colonial, cooperatively breeding fish Neolamprologus pulcher. Dominant males sired 76% of offspring in their group, whereas dominant females mothered 82% of offspring in their group. Subordinate reproduction was frequent, occurring in 47% of sampled groups. Subordinate males gained more paternity in groups located in high-density areas and in groups with many subordinate males. Dominant males and females in large groups and in groups with many reproductively mature subordinates had higher rates of parentage loss, but only at the colony edge. Our study provides, to our knowledge, the first comprehensive quantification of reproductive sharing among groups of wild N. pulcher, a model species for the study of cooperation and social behaviour. Further, we demonstrate that the frequency of extra-pair parentage differs across small social and spatial scales.     

Maternal risk of breeding failure remained low throughout the demographic transitions in fertility and age at first reproduction in Finland

Radical declines in fertility and postponement of first reproduction during the recent human demographic transitions have posed a challenge to interpreting human behaviour in evolutionary terms. This challenge has stemmed from insufficient evolutionary insight into individual reproductive decision-making and the rarity of datasets recording individual long-term reproductive success throughout the transitions. We use such data from about 2,000 Finnish mothers (first births: 1880s to 1970s) to show that changes in the maternal risk of breeding failure (no offspring raised to adulthood) underlay shifts in both fertility and first reproduction. With steady improvements in offspring survival, the expected fertility required to satisfy a low risk of breeding failure became lower and observed maternal fertility subsequently declined through an earlier age at last reproduction. Postponement of the age at first reproduction began when this risk approximated zero-even for mothers starting reproduction late. Interestingly, despite vastly differing fertility rates at different stages of the transitions, the number of offspring successfully raised to breeding per mother remained relatively constant over the period. Our results stress the importance of assessing the long-term success of reproductive strategies by including measures of offspring quality and suggest that avoidance of breeding failure may explain several key features of recent life-history shifts in industrialized societies.     

Male reproductive pattern in a polygynous ungulate with a slow life-history: the role of age, social status and alternative mating tactics

According to life-history theory age-dependent investments into reproduction are thought to co-vary with survival and growth of animals. In polygynous species, in which size is an important determinant of reproductive success, male reproduction via alternative mating tactics at young age are consequently expected to be the less frequent in species with higher survival. We tested this hypothesis in male Alpine ibex (Capra ibex), a highly sexually dimorphic mountain ungulate whose males have been reported to exhibit extremely high adult survival rates. Using data from two offspring cohorts in a population in the Swiss Alps, the effects of age, dominance and mating tactic on the likelihood of paternity were inferred within a Bayesian framework. In accordance with our hypothesis, reproductive success in male Alpine ibex was heavily biased towards older, dominant males that monopolized access to receptive females by adopting the ‘tending’ tactic, while success among young, subordinate males via the sneaking tactic ‘coursing’ was in general low and rare. In addition, we detected a high reproductive skew in male Alpine ibex, suggesting a large opportunity for selection. Compared with other ungulates with higher mortality rates, reproduction among young male Alpine ibex was much lower and more sporadic. Consistent with that, further examinations on the species level indicated that in polygynous ungulates the significance of early reproduction appears to decrease with increasing survival. Overall, this study supports the theory that survival prospects of males modulate the investments into reproduction via alternative mating tactics early in life. In the case of male Alpine ibex, the results indicate that their life-history strategy targets for long life, slow and prolonged growth and late reproduction.     

Sperm production and mating potential of males after a cold shock on pupae of the parasitoid wasp Dinarmus basalis (Hymenoptera: Pteromalidae)

For ectothermic species, temperature is a key environmental factor influencing several aspects of their physiology and ecology, acting particularly on reproduction. To measure the consequences of a severe thermal stress during development on male reproduction, a cold shock (1h at -18 degrees C) was tested on Dinarmus basalis pupae. D. basalis (Hymenoptera: Pteromalidae) is a parasitoid wasp in which sperm management in both male and female is of prime importance. After a cold shock, developmental success was reduced, with a quarter of cold-shocked males not emerging correctly. The stress effects were estimated at the level of sperm stock in seminal vesicles of males at different ages and on the ability of 2-day-old males to access females in single and multiple mating and in male-male competition. Cold-shocked males had a reduced sperm stock compared to control males and this difference persisted with age. The rate of sperm production was similar in both groups. The consequences of a cold shock on male reproductive ability were perceptible in multiple mating and male-male competition but not in single mating. Cold-shocked males were at a disadvantage, inseminating fewer females and copulating less frequently. Finally, male pupae of D. basalis were able to withstand severe temperature stresses and their reproductive functions were partially preserved.     

The influence of juvenile and adult environments on life-history trajectories

There is increasing evidence that the environment experienced early in life can strongly influence adult life histories. It is largely unknown, however, how past and present conditions influence suites of life-history traits regarding major life-history trade-offs. Especially in animals with indeterminate growth, we may expect that environmental conditions of juveniles and adults independently or interactively influence the life-history trade-off between growth and reproduction after maturation. Juvenile growth conditions may initiate a feedback loop determining adult allocation patterns, triggered by size-dependent mortality risk. I tested this possibility in a long-term growth experiment with mouthbrooding cichlids. Females were raised either on a high-food or low-food diet. After maturation half of them were switched to the opposite treatment, while the other half remained unchanged. Adult growth was determined by current resource availability, but key reproductive traits like reproductive rate and offspring size were only influenced by juvenile growth conditions, irrespective of the ration received as adults. Moreover, the allocation of resources to growth versus reproduction and to offspring number versus size were shaped by juvenile rather than adult ecology. These results indicate that early individual history must be considered when analysing causes of life-history variation in natural populations.     

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.     

Life-history variation following habitat degradation associated with differing fine-scale spatial genetic structure in a rainforest cycad

Habitat degradation can result in drastic environmental changes potentially affecting the life-history of populations and aspects of the reproductive biology and the genetic structure within and among populations. Here, we explore how life-history differences between subpopulations from contrasting habitats may affect mating availability, which in turn will indirectly affect the strength of spatial genetic structure within populations of a tropical rainforest cycad (Zamia fairchildiana). Subpopulations exposed to higher light availability in degraded-forest habitats had male individuals that grew faster, reproduced earlier, and invested more in reproduction than in native-forest habitat subpopulations. These differences in life history resulted in degraded-habitat subpopulations showing a higher proportion of reproductive adults and greater mate availability in a reproductive season. Subpopulations in the degraded habitat showed weaker SGS, i.e., a smaller slope in the linear regression of genetic relatedness on linear distance. Environmentally induced changes in life history and subsequent changes in the strength of the SGS after habitat degradation may have important consequences for population viability and should be of concern in conservation.     

The Effects of Within- and Between-Group Competition on Trust and Trustworthiness among Acquaintances

Several studies have indicated that between-group competition is a key stimulator of trust and trustworthiness. Another important but neglected type of competition may also affect trust and trustworthiness: within-group competition, especially competition among acquaintances. The present study investigated the effects of both within- and between-group competition on trust and trustworthiness, which were measured using an investment game played by acquaintances. We found that, compared to the participants'' performance in the non-competition condition, when individuals were motivated to compete with their in-group members or the other groups for financial rewards, they demonstrated more trust. When individuals were motivated to compete with their in-group members, they exhibited lower trustworthiness than in non-competition and between-group competition. In addition, within-group competition decreased the trustor''s payoff while both within- and between- group competition increased the trustee''s payoff. Finally, we found that males trusted their group members more than females.     

The Persistence of Facultative Parthenogenesis in Drosophila albomicans

Parthenogenesis has evolved independently in more than 10 Drosophila species. Most cases are tychoparthenogenesis, which is occasional or accidental parthenogenesis in normally bisexual species with a low hatching rate of eggs produced by virgin females; this form is presumed to be an early stage of parthenogenesis. To address how parthenogenesis and sexual reproduction coexist in Drosophila populations, we investigated several reproductive traits, including the fertility, parthenogenetic capability, diploidization mechanisms, and mating propensity of parthenogenetic D. albomicans. The fertility of mated parthenogenetic females was significantly higher than that of virgin females. The mated females could still produce parthenogenetic offspring but predominantly produced offspring by sexual reproduction. Both mated parthenogenetic females and their parthenogenetic-sexual descendants were capable of parthenogenesis. The alleles responsible for parthenogenesis can be propagated through both parthenogenesis and sexual reproduction. As diploidy is restored predominantly by gamete duplication, heterozygosity would be very low in parthenogenetic individuals. Hence, genetic variation in parthenogenetic genomes would result from sexual reproduction. The mating propensity of females after more than 20 years of isolation from males was decreased. If mutations reducing mating propensities could occur under male-limited conditions in natural populations, decreased mating propensity might accelerate tychoparthenogenesis through a positive feedback mechanism. This process provides an opportunity for the evolution of obligate parthenogenesis. Therefore, the persistence of facultative parthenogenesis may be an adaptive reproductive strategy in Drosophila when a few founders colonize a new niche or when small populations are distributed at the edge of a species'' range, consistent with models of geographical parthenogenesis.