Do Early-Life Conditions Drive Variation in Senescence of Female Bighorn Sheep?

The rate of senescence may vary among individuals of a species according to individual life histories and environmental conditions. According to the principle of allocation, changes in mortality driven by environmental conditions influence how organisms allocate resources among costly functions. In several vertebrates, environmental conditions during early life impose trade-offs in allocation between early reproduction and maintenance. The effects of conditions experienced during early life on senescence, however, remain poorly documented in wild populations. We examined how several early-life environmental conditions affected reproductive and survival senescence in wild bighorn sheep. We found long-term effects of high population density at birth, precipitations during the winter before birth, and temperature during the winter following birth that decreased survival after 7 years of age. High temperature during the first summer and autumn of life and high Pacific decadal oscillation decreased reproductive success at old ages. However, harsh early-life environment did not influence the rate of senescence in either survival or reproduction. Contrary to our expectation, we found no trade-off between reproductive allocation prior to senescence and senescence. Our results do show that early-life environmental conditions are important drivers of later survival and reproductive success and contribute to intra-specific variation in late-life fitness, but not aging patterns. These conditions should therefore be considered when studying the mechanisms of senescence and the determinants of variation in both survival and reproductive senescence at older ages.

Flexibility Is Costly: Hidden Physiological Damage From Seasonal Phenotypic Transitions in Heterothermic Species.

Heterothermy allows organisms to cope with fluctuating environmental conditions. The use of regulated hypometabolism allows seasonal heterothermic species to cope with annual resource shortages and thus to maximize survival during the unfavorable season. This comes with deep physiological remodeling at each seasonal transition to allow the organism to adjust to the changing environment. In the wild, this adaptation is highly beneficial and largely overcomes potential costs. However, researchers recently proposed that it might also generate both ecological and physiological costs for the organism. Here, we propose new perspectives to be considered when analyzing adaptation to seasonality, in particular considering these costs. We propose a list of putative costs, including DNA damage, inflammatory response to fat load, brain and cognitive defects, digestive malfunction and immunodeficiency, that should receive more attention in future research on physiological seasonality. These costs may only be marginal at each transition event but accumulate over time and therefore emerge with age. In this context, studies in captivity, where we have access to aging individuals with limited extrinsic mortality (e.g., predation), could be highly valuable to experimentally assess the costs of physiological flexibility. Finally, we offer new perspectives, which should be included in demographic models, on how the adaptive value of physiological flexibility could be altered in the future in the context of global warming.

Female reproduction bears no survival cost in captivity for gray mouse lemurs.

The survival cost of reproduction has been revealed in many free-ranging vertebrates. However, recent studies on captive populations failed to detect this cost. Theoretically, this lack of survival/reproduction trade-off is expected when resources are not limiting, but these studies may have failed to detect the cost, as they may not have fully accounted for potential confounding effects, in particular interindividual heterogeneity. Here, we investigated the effects of current and past reproductive effort on later survival in captive females of a small primate, the gray mouse lemur. Survival analyses showed no cost of reproduction in females; and the pattern was even in the opposite direction: the higher the reproductive effort, the higher the chances of survival until the next reproductive event. These conclusions hold even while accounting for interindividual heterogeneity. In agreement with aforementioned studies on captive vertebrates, these results remind us that reproduction is expected to be traded against body maintenance and the survival prospect only when resources are so limiting that they induce an allocation trade-off. Thus, the cost of reproduction has a major extrinsic component driven by environmental conditions.

Trophy hunting mediates sex-specific associations between early-life environmental conditions and adult mortality in bighorn sheep.

Environmental conditions during early development, from conception to sexual maturity, can have lasting consequences on fitness components. Although adult life span often accounts for much of the variation in fitness in long-lived animals, we know little about how early environment affects adult life span in the wild, and even less about whether these effects differ between the sexes. Using data collected over 45 years from wild bighorn sheep (Ovis canadensis), we investigated the effects of early environment on adult mortality in both sexes, distinguishing between natural and anthropogenic sources of mortality. We used the average body mass of yearlings (at about 15 months of age) as a yearly index of environmental quality. We first examined sex differences in natural mortality responses to early environment by censoring harvested males in the year they were shot. We then investigated sex differences in the effects of early environment on overall mortality (natural and hunting mortality combined). Finally, we used path analysis to separate the direct influence of early environment from indirect influences, mediated by age at first reproduction, adult mass and horn length. As early environmental conditions improved, natural adult mortality decreased in both sexes, although for males the effect was not statistically supported. Sex differences in the effects of early environment on adult mortality were detected only when natural and hunting mortality were pooled. Males that experienced favourable early environment had longer horns as adults and died earlier because of trophy hunting, which does not mimic natural mortality. Females that experienced favourable early environment started to reproduce earlier and early primiparity was associated with reduced mortality, suggesting a silver-spoon effect. Our results show that early conditions affect males and females differently because of trophy hunting. These findings highlight the importance of considering natural and anthropogenic environmental factors across different life stages to understand sex differences in mortality.

Long-term prevalence data reveals spillover dynamics in a multi-host (Artemia), multi-parasite (Microsporidia) community.

In the study of multi-host parasites, it is often found that host species contribute asymmetrically to parasite transmission. Yet in natural populations, identifying which hosts contribute to parasite transmission and maintenance is a recurring challenge. Here, we approach this issue by taking advantage of natural variation in the composition of a host community. We studied the brine shrimps Artemia franciscana and Artemia parthenogenetica and their microsporidian parasites Anostracospora rigaudi and Enterocytospora artemiae. Previous laboratory experiments had shown that each host can transmit both parasites, but could not predict their actual contributions to the parasites' maintenance in the field. To resolve this, we gathered long-term prevalence data from a metacommunity of these species. Metacommunity patches could contain either or both of the Artemia host species, so that the presence of the hosts could be linked directly to the persistence of the parasites. First, we show that the microsporidian A. rigaudi is a spillover parasite: it was unable to persist in the absence of its maintenance host A. parthenogenetica. This result was particularly striking, as A. rigaudi displayed both high prevalence (in the field) and high infectivity (when tested in the laboratory) in both hosts. Moreover, the seasonal presence of A. parthenogenetica imposed seasonality on the rate of spillover, causing cyclical pseudo-endemics in the spillover host A. franciscana. Second, while our prevalence data was sufficient to identify E. artemiae as either a spillover or a facultative multi-host parasite, we could not distinguish between the two possibilities. This study supports the importance of studying the community context of multi-host parasites, and demonstrates that in appropriate multi-host systems, sampling across a range of conditions and host communities can lead to clear conclusions about the drivers of parasite persistence.

Offspring mass variation in tree swallows: A case of bet-hedging?

The evolution of reproductive strategies is affected by the ability of organisms to deal with future environmental conditions. When environments are temporally unpredictable, however, it is difficult to anticipate optimal offspring phenotype. Diversification of offspring phenotypes, a strategy called diversified bet-hedging, may allow parents to maximize their fitness by reducing between-year variation in reproductive success. The link between diversification of offspring phenotypes and individual reproductive success, however, has rarely been documented empirically. We used an eight-year dataset (1215 broods, 870 females) on individually marked tree swallows (Tachycineta bicolor) to assess whether intra-brood mass variation was compatible with a diversified bet-hedging strategy. Intra-brood mass variation was weakly, but significantly repeatable within females, suggesting consistent individual differences. Greater intra-brood mass variation, however, was not associated with reduced between-year variation in reproductive success or increased female reproductive success. Moreover, contrary to diversified bet-hedging expectations, fledging success of large broods was greater when hatchlings had similar rather than variable masses. Our results suggest that intra-brood mass variation may not result from diversified bet-hedging, but rather from complex interactions between environmental, brood, and maternal characteristics.

State transitions: a major mortality risk for seasonal species.

Ageing results from the accumulation of multifactorial damage over time. However, the temporal distribution of this damage remains unknown. In seasonal species, transitions between seasons are critical periods of massive physiological remodelling. We hypothesised that these recurrent peaks of physiological remodelling are costly in terms of survival. We tested whether captive small primates exposed to an experimentally increased frequency of seasonal transitions die sooner than individuals living under natural seasonality. The results show that experiencing one additional season per year increases the mortality hazard by a factor of 3 to 4, whereas the expected number of seasons lived is only slightly impacted by the seasonal rhythm. These results demonstrate that physiological transitions between periods of high and low metabolic activity represent a major mortality risk for seasonal organisms, which has been ignored until now.

Cytological, molecular and life cycle characterization of Anostracospora rigaudi n. g., n. sp. and Enterocytospora artemiae n. g., n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia.

Two new microsporidia, Anostracospora rigaudi n. g., n. sp., and Enterocytospora artemiae n. g., n. sp. infecting the intestinal epithelium of Artemia parthenogenetica Bowen and Sterling, 1978 and Artemia franciscana Kellogg, 1906 in southern France are described. Molecular analyses revealed the two species belong to a clade of microsporidian parasites that preferentially infect the intestinal epithelium of insect and crustacean hosts. These parasites are morphologically distinguishable from other gut microsporidia infecting Artemia. All life cycle stages have isolated nuclei. Fixed spores measure 1·3×0·7 µm with 5-6 polar tube coils for A. rigaudi and 1·2×0·9 µm with 4 polar tube coils for E. artemiae. Transmission of both species is horizontal, most likely through the ingestion of spores released with the faeces of infected hosts. The minute size of these species, together with their intestinal localization, makes their detection and identification difficult. We developed two species-specific molecular markers allowing each type of infection to be detected within 3-6 days post-inoculation. Using these markers, we show that the prevalence of these microsporidia ranges from 20% to 75% in natural populations. Hence, this study illustrates the usefulness of molecular approaches to study prevalent, but cryptic, infections involving microsporidian parasites of gut tissues.