Sex-biased terminal investment in offspring induced by maternal immune challenge in the house wren (Troglodytes aedon)

The reproductive costs associated with the upregulation of immunity have been well-documented and constitute a fundamental trade-off between reproduction and self-maintenance. However, recent experimental work suggests that parents may increase their reproductive effort following immunostimulation as a form of terminal parental investment as prospects for future reproduction decline. We tested the trade-off and terminal investment hypotheses in a wild population of house wrens (Troglodytes aedon) by challenging the immune system of breeding females with lipopolysaccharide, a potent but non-lethal antigen. Immunized females showed no evidence of reproductive costs; instead, they produced offspring of higher phenotypic quality, but in a sex-specific manner. Relative to control offspring, sons of immunized females had increased body mass and their sisters exhibited higher cutaneous immune responsiveness to phytohaemagglutinin injection, constituting an adaptive strategy of sex-biased allocation by immune-challenged females to enhance the reproductive value of their offspring. Thus, our results are consistent with the terminal investment hypothesis, and suggest that maternal immunization can induce pronounced transgenerational effects on offspring phenotypes.     

Reproductive success in presenescent common gulls (Larus canus): the importance of the last year of life

Survival selection against individuals of inferior quality (measured as breeding success) has been proposed to account for the increase in average reproductive success with advancing age in presenescent birds. This so-called selection hypothesis relies on quality-dependent survival. In the present breeding performance study of common gulls, Larus canus, this assumption was not verified. In particular, omitting the last breeding year from the analysis resulted in the disappearance of the correlation between breeding success and survival. A positive correlation in the full dataset was thus solely based on the poor breeding success of ultimate breeders. Indeed, presenescent individuals were shown to have a specifically low breeding success in their terminal breeding event. The poor success of ultimate breeders thus reflects an abruptly declined condition rather than the birds' overall quality. A comparison of the survival of poor and good performers, involving last-time breeders, thus needs not to be a proper test of the selection hypothesis. Longitudinal analysis revealed a steady increase of individual breeding success until the tenth breeding year. The results suggest that an increase of breeding success with age often found in cross-sectional analyses is primarily a result of age-related improvements of competence and/or increased reproductive effort.     

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.     

Experience versus effort: what explains dynamic heterogeneity with respect to age?

Age‐related patterns of survival and reproduction have been explained by accumulated experience (‘experience hypothesis’), increased effort (‘effort hypothesis’), and intrinsic differences in phenotypes (‘selection hypothesis’). We examined the experience and effort hypotheses using a 40‐year data set in a population of Leach's storm‐petrels Oceanodroma leucorhoa, long‐lived seabirds for which the effect of phenotypic variation has been previously demonstrated. Age was quantified by time since recruitment (‘breeding age’). The best model of adult survival included a positive effect of breeding age (1, 2, 3+ years), sex (male > female), and year. Among‐individuals variation (fixed heterogeneity) accounted for 31.6% of the variance in annual reproductive success. We further examined within‐individual patterns in reproductive success (dynamic heterogeneity) in the subset of individuals with at least five breeding attempts. Three distinct phases characterized reproductive success – early increase, long asymptotic peak, late decline. No effect of early reproductive output on longevity was found, however, early success was positively correlated with lifetime reproductive success. Reproductive success was lower earlier than later in life. Among the few natally philopatric individuals in the population, age of first breeding had no effect on longevity, lifetime reproductive success, or early reproductive success. No support for the effort hypothesis was found in this population. Instead, age‐specific patterns of survival and reproduction in these birds are best explained by the experience hypothesis over and above the effect of intrinsic differences among individuals.     

Maternal effort and male quality in the bank vole, Clethrionomys glareolus.

Parental investment in reproduction is adjusted according to potential benefits in terms of offspring survival and/or mating success. If male quality affects the reproductive success of a female, then females mating with high-quality males should invest more in reproduction. Although the subject has been of general interest, further experimental verification of the hypothesis is needed. We studied whether female bank voles (Clethrionomys glareolus) adjusted their maternal effort according to male quality, measured as mating success. To enable the measurement of maternal effort during nursing separately from male genetic effects the litters were cross-fostered. Further, the genetic background of male quality was examined. Male quality did not correlate with litter size or offspring size at birth. Offspring growth was positively related to food consumption and milk production of mothers. However, these direct measurements of maternal effort were independent of male quality. Male mating success appeared to be significantly heritable indicating that there are genetic benefits. Still, females did not adjust maternal effort according to the genetic quality of their offspring. We suggest that female bank voles gain significant genetic benefits from mating with high-quality males whereas they cannot improve their reproductive success by increasing maternal effort.     

Age-related patterns of reproductive success in house sparrows Passer domesticus

A common life history pattern in many organisms is that reproductive success increases with age. We report a similar pattern in house sparrows Passer domesticus , older individuals performed better than yearlings for most measures of reproductive success. Older males and females began breeding earlier in a given season and fledged more young than their yearling counterparts. Individual males also fledged more young in their second breeding season than they did in their first, but individual females did not show consistent improvement in reproductive success from year one to two. A path analysis indicated that age in both sexes acted primarily through the timing of breeding; earlier nesters laid more eggs and hence fledged more young but did not have more nesting attempts. We tested whether the increased reproductive success with age arose from high quality individuals surviving to be older (selection hypothesis). In contrast to the main prediction of this hypothesis that reproductive success and survival should be positively related, we found that survival from one year of age to two years of age was negatively related to reproductive success in the first year for males and females combined. Additionally, individuals that survived to breed as two-year-olds did not differ in total young fledged in their first year from those that did not survive to their second season of breeding. Our results indicate that fledgling production increases with age due to improvements in timing of breeding, particularly in females, and not because of the loss of poor breeders or increased output. Mechanisms producing age-related differences in timing of breeding warrant further study.     

Age- and density-dependent reproductive effort in male red deer

Reproductive effort in female ungulates originates from gestation and lactation and has been studied extensively; however, no comparable studies of reproductive effort in males (due to fighting for access to mates) have, to our knowledge, previously been reported. Here, we report on weight loss of male red deer during the annual mating season--a direct measure of male reproductive effort (or somatic reproductive costs). The 'terminal investment' hypothesis predicts that reproductive effort should increase with age, given that costs remain stable. We also propose the 'mating strategy-effort' hypothesis, which predicts that reproductive effort peaks in prime-aged males, since they are most often the harem holders. Consistent with the mating strategy-effort hypothesis, relative weight loss during the rutting season peaked at prime age and was lower in younger and senescent males. Weight loss during the rut was relatively smaller as density increased and more so for older males. This is probably primarily due to males (particularly senescent males) starting their rut in poorer condition at high density. The pattern of reproductive effort in males with regard to age and density therefore differs markedly from the pattern reported for females.     

Immune system activation interacts with territory-holding potential and increases predation of the damselfly Calopteryx splendens by birds

Activation of the immune system in insects has been shown to be costly in the laboratory setting, but experimental studies in the field are lacking. The costs of immunity in the wild may be different to those in the laboratory because animals in the wild are simultaneously subjected to a suite of selective agents. We have measured the costs of immune system activation in a wild population of the territorial damselfly Calopteryx splendens. Immune-challenged males were found to be less likely to be territorial and had lower overall survival rates than control or sham-manipulated males. Because territorial males have a higher mating success than nonterritorial males, this result suggests that immune-challenged males are also likely to suffer reduced mating success. However, the activation of the immune system as such did not increase predation risk; this occurred due to a combination of the former with a reduced territory-holding potential. As such, immune-challenged males not holding a territory were most susceptible to predation by birds. The size of the wing spots, a known sexually selected male trait, predicted territorial behaviour in control and sham-manipulated males, but not in immune-challenged males. Our data show that immune system activation can have several costs acting in unison and that ubiquitous ecological interactions, such as predation, may affect trade-offs between immunity and other life history traits.     

Calling,Courtship, and Condition in the Fall Field Cricket,Gryllus pennsylvanicus

Theoretically, sexual signals should provide honest information about mating benefits and many sexually reproducing species use honest signals when signalling to potential mates. Male crickets produce two types of acoustic mating signals: a long-distance mate attraction call and a short-range courtship call. We tested whether wild-caught fall field cricket (Gryllus pennsylvanicus) males in high condition (high residual mass or large body size) produce higher effort calls (in support of the honest signalling hypothesis). We also tested an alternative hypothesis, whether low condition males produce higher effort calls (in support of the terminal investment hypothesis). Several components of long-distance mate attraction calls honestly reflected male body size, with larger males producing louder mate attraction calls at lower carrier frequencies. Long-distance mate attraction chirp rate dishonestly signalled body size, with small males producing faster chirp rates. Short-range courtship calls dishonestly reflected male residual mass, as chirp rate and pulse rate were best explained by a curvilinear function of residual mass. By producing long-distance mate attraction calls and courtship calls with similar or higher effort compared to high condition males, low condition males (low residual mass or small body size) may increase their effort in current reproductive success at the expense of their future reproductive success, suggesting that not all sexual signals are honest.     

Age‐Related Male Reproductive Investment in Courtship Display and Nuptial Gifts in a Moth,Ostrinia scapulalis

Due to a trade‐off between current and future reproduction, costly reproductive investments should be increased towards the end of a lifespan when the probability of reproduction becomes low (terminal investment hypothesis). We investigated age‐related changes in male reproductive investment towards courtship display and the spermatophore in three age classes (young, middle‐aged and old) of a monandrous moth, Ostrinia scapulalis. As predicted, old males had higher mating success than young and middle‐aged males in no‐choice tests. Moreover, two‐choice tests revealed that middle‐aged males had a higher success rate than young males because of their higher courtship frequency rather than any female preference for them. It was found that old males produced a larger spermatophore than young and middle‐aged males, suggesting greater reproductive effort. The protein content of spermatophores also tended to increase with male age. Despite the age‐related variation in spermatophore size and protein content, age did not affect female fecundity or longevity. A decrease in the number of sperm in the older males might counteract the nutritional benefit of larger spermatophores. Alternatively, fitness components other than longevity and fecundity may be influenced by male age.     

Age-specific mating strategies and reproductive senescence

While males gain obvious direct advantages from multiple mating, the reproductive capacity of females is more constrained. The reason why polyandry evolved in females is therefore open to many conjectures. One hypothesis postulates that females gain indirect benefits by increasing the probability of siring young from high quality males. To explore this hypothesis, we used the natural variation of the reproductive value that males and females undergo through age. The age-related variation of phenotypic performance might then induce variations in mating strategies in males and females. Using the common lizard (Lacerta vivipara) as our model system, we showed that reproductive immaturity and senescence created variability in both male and female reproductive success (including survival of offspring). Consistent with theory, males at their best-performing phenotype adopted a polygynous strategy. These males were of an intermediate age and they produced offspring of higher viability than younger and older males. In contrast, females at their best performing phenotype, also of an intermediate age, were less polyandrous than other less-performing females. Middle-aged females tended to mate with males of an intermediate age and produced litters with higher viability independently from their reproductive strategy. Males of an intermediate age enhanced their fitness by additional matings with young or old females. Young and old females increased their fitness by being more polyandrous. Polyandry therefore appears as means to seek for good males. A positive correlation between males and their partners' fitness disagree with the idea that polyandry is the result of a sexual conflict in this species.     

Transgenerational interactions involving parental age and immune status affect female reproductive success in Drosophila melanogaster

It is well established that the parental phenotype can influence offspring phenotypic expression, independent of the effects of the offspring''s own genotype. Nonetheless, the evolutionary implications of such parental effects remain unclear, partly because previous studies have generally overlooked the potential for interactions between parental sources of non-genetic variance to influence patterns of offspring phenotypic expression. We tested for such interactions, subjecting male and female Drosophila melanogaster of two different age classes to an immune activation challenge or a control treatment. Flies were then crossed in all age and immune status combinations, and the reproductive success of their immune- and control-treated daughters measured. We found that daughters produced by two younger parents exhibited reduced reproductive success relative to those of other parental age combinations. Furthermore, immune-challenged daughters exhibited higher reproductive success when produced by immune-challenged relative to control-treated mothers, a pattern consistent with transgenerational immune priming. Finally, a complex interplay between paternal age and parental immune statuses influenced daughter''s reproductive success. These findings demonstrate the dynamic nature of age- and immune-mediated parental effects, traceable to both parents, and regulated by interactions between parents and between parents and offspring.     

Female access and diet affect insemination success,senescence and the cost of reproduction in the male Mexican fruit fly Anastrepha ludens

Hypotheses exploring the influence of dietary conditions on the life‐history trade‐off between survival and reproductive success are extensively tested in female insects but only rarely explored in males. The present study examines the impact of dietary quality and female access on age‐specific reproduction and survival of the male Mexican fruit fly Anastrepha ludens Loew (Diptera: Tephritidae). There is a clear cost of female access for males with access to dietary protein, measurable as a decrease in life expectancy, which is further influenced by the age when females are introduced. A protein deficient diet reduces the lifespan benefit of virginity and masks the detrimental effect of female access on male life expectancy. Dietary protein is not necessary for reproductive success, although access to protein at eclosion improves the lifetime reproductive success of males compared to when it is delayed. Overall, reproductive success diminishes as the male flies age, regardless of the dietary conditions, providing evidence for reproductive senescence in males. Delaying the males' access to a protein source fails to influence the negative effect of age on reproductive ability. Because age‐specific reproductive rates decline with age, regardless of diet, male fitness does not benefit from lifespan extension. Therefore, males can be expected to allocate available resources towards reproductive effort in favour of an extended lifespan, regardless of mate and protein availability.     

BODY SIZE AND HAREM SIZE IN MALE RED-WINGED BLACKBIRDS: MANIPULATING SELECTION WITH SEX-SPECIFIC FEEDERS

We experimentally manipulated the strength of selection in the field on red-winged blackbirds (Agelaius phoeniceus) to test hypotheses about contrasting selective forces that favor either large or small males in sexually size dimorphic birds. Selander (1972) argued that sexual selection favors larger males, while survival selection eventually stabilizes male size because larger males do not survive as well as smaller males during harsh winters. Searcy (1979a) proposed instead that sexual selection may be self limiting: male size might be stabilized not by overwinter mortality, but by breeding-season sexual selection that favors smaller males. Under conditions of energetic stress, smaller males should be able to display more and thus achieve higher reproductive success. Using feeders that provisioned males or females but not both, we produced conditions that mimicked the extremes of natural conditions. We found experimental support for the hypothesis that when food is abundant, sexual selection favors larger males. But even under conditions of severe energetic stress, smaller males did not gain larger harems, as the self-limiting hypothesis predicted. Larger males were more energetically stressed than smaller males, but in ways that affected their future reproductive output rather than their current reproductive performance. Stressed males that returned had smaller wings and tails than those that did not return; among returning stressed males, relative harem sizes were inversely related to wing and tail length. Thus, male body size may be stabilized not by survival costs during the non-breeding season, nor by energetic costs during the breeding season, but by costs of future reproduction that larger males pay for their increased breeding-season effort.     

Survival costs of reproduction in the blue tit (Parus caeruleus): a role for blood parasites?

One of the central tenets in life-history theory is that there is a trade-off between current and future reproduction (i.e. a cost of reproduction). The mechanism for this cost of reproduction is, however, largely unknown. One hypothesis is that the high workload during reproduction compromises resistance to parasites and that the resulting increase in parasitaemia has negative effects on the prospects of future survival. Although empirical evidence for a negative relationship between reproductive effort and parasite resistance exists, the causal relationships between reproductive effort, parasite resistance and future reproduction are still unclear. We use a path analytical approach to investigate whether a change in parasite resistance (as measured by intensities of infections by the blood parasite Haemoproteus) after manipulation of reproductive effort, translates into altered survival in female blue tits. Our results show a negative relationship between reproductive effort and parasite resistance, although evident only in first-year breeders. Moreover, we found survival costs of reproduction in first-year breeders. These costs were, however, not mediated by the blood parasite studied.     

Reproduction under predation risk and the trade-off between current and future reproduction in the threespine stickleback

An increasing number of studies show that animals adjust their reproductive effort to the risk of predation. However, to maximize lifetime reproductive success this adjustment should depend on the animals'' current and future reproductive potential. Here I tested this hypothesis by allowing threespine stickleback males (Gasterosteus aculeatus), differing in current and future mating probabilities, to reproduce in pools in both the presence and absence of predators. As expected, males adjusted their reproductive effort to the risk of predation. Fewer males bred, and all males developed less nuptial coloration in the presence of predators. However, males with a low current mating probability took less risk than males with a higher mating probability, whereas all males increased risk taking when future reproductive opportunities decreased. The results thus support the hypothesis that males are able to assess both the risk of predation and their current versus future mating probability, and adjust their reproductive decisions accordingly. The study further suggests that predation risk may have less effect on sexual selection than previously assumed, as the males which refrained from reproducing in the presence of predators were mainly males with a low mating probability.     

Age‐specific reproduction and disposable soma in an urban population of Common Blackbirds Turdus merula

The mechanism of senescence is an important subject of current research, but our knowledge of the factors influencing the rate of ageing in naturally occurring populations remains rudimentary. Evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance and thus result in earlier or more rapid senescence. We use data on the complete reproductive histories of 431 Common Blackbirds (222 males and 209 females) collected during a 19‐year study of the ecology of an urban population of this species to test the main hypotheses addressing the issue of senescence. On average, the birds in this population survived for 3.7 (± 1.9 sd) years. Reproductive success in females peaked at the age of 4, but in males remained stable until the 5th year of life. We observed declines in reproductive success, indicative of senescence, after the peak years in both sexes. The mechanism of age‐related changes in the reproduction of females confirms the individual improvement and selective disappearance hypotheses. In the case of males, the increase in reproductive performance comes as a consequence of the disappearance of poor reproducers. The parental investment associated with early life fecundity (the first two breeding seasons in males and females) impairs the breeding success of females later on. Contrary to expectations, there was no negative impact of high early life fecundity on either mortality or lifespan. Individuals of both sexes with a high early life fecundity had a higher lifetime reproductive success than those in which early life fecundity was low. Hence, the most profitable strategy is to maximize reproductive effort in the early stages of life. This yields the highest lifetime reproductive success, despite the increased impact of senescence, especially in females. These results are consistent with the disposable soma hypothesis.     

Testosterone levels of free-ranging resident mantled howler monkey males in relation to the number and density of solitary males: a test of the challenge hypothesis

The challenge hypothesis asserts that testosterone levels and aggression in male adult animals are closely associated with one another in the context of intense reproductive competition, particularly when males challenge one another for the access to females. For mantled howler monkeys (Alouatta palliata), the presence of a solitary male in the vicinity of a social group can be considered a threat for the reproductive success of the resident males, as group takeovers by solitary males are followed by a reestablishment of the access to females among group males and sometimes by infanticide. Therefore, these episodes should be accompanied by an increase in testosterone secretion according to the challenge hypothesis. In order to test our prediction, we relate different group and subpopulation variables to the testosterone levels measured in feces collected from 10 groups living in 6 forest fragments, at Los Tuxtlas, Mexico. Our results suggest that resident A. palliata males regard solitary individuals as potential contesters for their reproductive success and that they respond to interactions with them with an increase in testosterone levels, that is increasing their aggressiveness. Our results also suggest that in the studied groups all males have at least certain access to mates and that the entrance of a new male would affect their reproductive success negatively. Finally, the negative effects of chronically high testosterone levels may be negatively affecting the fitness of our study groups living in high population densities and small fragments.     

Terminal investment in the gustatory appeal of nuptial food gifts in crickets

Investment in current versus future reproduction represents a prominent trade‐off in life‐history theory and is likely dependent on an individual's life expectancy. The terminal investment hypothesis posits that a reduction in residual reproductive value (i.e. potential for future offspring) will result in increased investment in current reproduction. We tested the hypothesis that male decorated crickets (Gryllodes sigillatus), when cued to their impending mortality, should increase their reproductive effort by altering the composition of their nuptial food gifts (i.e. spermatophylaxes) to increase their gustatory appeal to females. Using a repeated‐measures design, we analysed the amino acid composition of spermatophylaxes derived from males both before and after injection of either a saline control or a solution of heat‐killed bacteria. The latter, although nonpathogenic, represents an immune challenge that may signal an impending survival threat. One principal component explaining amino acid variation in spermatophylaxes, characterized by a high loading to histidine, was significantly lower in immune‐challenged versus control males. The relevance of this difference for the gustatory appeal of gifts to females was assessed by mapping spermatophylax composition onto a fitness surface derived in an earlier study identifying the amino acid composition of spermatophylaxes preferred by females. We found that immune‐challenged males maintained the level of attractiveness of their gifts post‐treatment, whereas control males produced significantly less attractive gifts post‐injection. These results are consistent with the hypothesis that cues of a survival‐threatening infection stimulate terminal investment in male decorated crickets with respect to the gustatory appeal of their nuptial food gifts.     

Song strophe-length and reproductive success in a non-passerine bird, the Hoopoe Upupa epops

Hoopoe Upupa epops males produce a very simple song, with a repertoire size of one, in which the main difference between different strophes of a male and between the songs of different males is the number of elements they include (strophe-length). In several passerine species it has been shown that strophe-length is a sexually selected trait that reflects male quality and correlates with reproductive success. Here we analyse whether in a non-passerine, the Hoopoe, strophe-length of males is correlated with several variables of their reproductive success. Females paired with males singing long strophes laid their first clutch earlier, produced larger first clutches and laid second clutches after a successful first one more frequently than those paired with males singing short strophes. Moreover, males with long strophes produced more fledglings in their first clutches and in the whole season, partly because they brought more food for the brood than males with short strophes. The relationships found are not mediated by age effects. Previously we have shown that Hoopoe females in the early spring are attracted preferentially to songs with long strophes. Here we show that males singing long strophes also obtain postpairing benefits in terms of reproductive success, and that females paired with these males obtain direct benefits because these males provide greater feeding effort in the second half of the nestling period. These findings support the hypothesis that in the Hoopoe, strophe-length is a sexually selected cue under direct selection.