Sex differences in condition dependence of natal dispersal in a large herbivore: dispersal propensity and distance are decoupled.

Evolution should favour plasticity in dispersal decisions in response to spatial heterogeneity in social and environmental contexts. Sex differences in individual optimization of dispersal decisions are poorly documented in mammals, because species where both sexes commonly disperse are rare. To elucidate the sex-specific drivers governing dispersal, we investigated sex differences in condition dependence in the propensity and distance of natal dispersal in one such species, the roe deer, using fine-scale monitoring of 146 GPS-collared juveniles in an intensively monitored population in southwest France. Dispersal propensity increased with body mass in males such that 36% of light individuals dispersed, whereas 62% of heavy individuals did so, but there was no evidence for condition dependence in dispersal propensity among females. By contrast, dispersal distance increased with body mass at a similar rate in both sexes such that heavy dispersers travelled around twice as far as light dispersers. Sex differences in the strength of condition-dependent dispersal may result from different selection pressures acting on the behaviour of males and females. We suggest that females disperse prior to habitat saturation being reached, likely in relation to the risk of inbreeding. By contrast, natal dispersal in males is likely governed by competitive exclusion through male-male competition for breeding opportunities in this strongly territorial mammal. Our study is, to our knowledge, a first demonstration that condition dependence in dispersal propensity and dispersal distance may be decoupled, indicating contrasting selection pressures drive the behavioural decisions of whether or not to leave the natal range, and where to settle.

Does body growth impair immune function in a large herbivore?

According to the principle of allocation, trade-offs are inevitable when resources allocated to one biological function are no longer available for other functions. Growth, and to a lesser extent, immunity are energetically costly functions that may compete with allocation to reproductive success and survival. However, whether high allocation to growth impairs immune system development during the growing period or immune system performance during adulthood is currently unknown in wild mammals. Using three roe deer (Capreolus capreolus) populations experiencing contrasting environmental conditions, we tested for potential costs of growth on immune phenotype over both the short-term (during growth), and the long-term (during adulthood) over the course of an individuals' life. We investigated potential costs on a set of 12 immune traits that reflect both innate and adaptive responses, and compared them between sexes and populations. Although fast growth tended to be associated with low levels of some humoral traits (globulins) during the growing period and some cellular immune traits (i.e. eosinophil and neutrophil counts) during adulthood, evidence for a trade-off between growth and other immune components was limited. Unexpectedly, no detectable growth costs on immunity were found in females from the population experiencing the least favourable environment. We discuss our findings in the light of the complex interplay between resource allocation strategies among reproduction, maintenance and immunity, in relation to local environmental conditions experienced by roe deer.

Between-population differences in the genetic and maternal components of body mass in roe deer.

BACKGROUND: Understanding the genetic and environmental mechanisms governing variation in morphology or phenology in wild populations is currently an important challenge. While there is a general consensus that selection is stronger under stressful conditions, it remains unclear whether the evolutionary potential of traits should increase or decrease with increasingly stressful conditions. Here, we investigate how contrasting environmental conditions during growth may affect the maternal and genetic components of body mass in roe deer, the most abundant and widespread wild ungulate in Western Europe. Body mass is a key life history trait that strongly influences both survival and reproductive performance in large herbivores. We used pedigrees and animal models to determine the variance components of juvenile and adult winter body mass in two populations experiencing contrasting early-life conditions. RESULTS: Our analyses showed that roe deer at Chizé, where habitat was poor and unpredictable, exhibited very low genetic variance in juvenile body mass. Instead, variance in mass was mainly driven by among-cohort differences in early-life conditions and maternal environment. In contrast, roe deer at Bogesund, where resource availability during the critical period of fawn rearing was higher, displayed a substantial level of genetic variance in body mass. We discuss the potential role of past demography and viability selection on fawn body mass on the erosion of genetic variance in the poor habitat. CONCLUSIONS: Our study highlights the importance of accounting for both spatial (i.e. between-population variation) and temporal (i.e. cohort variation) heterogeneity in environmental conditions, especially in early life, to understand the potential for adaptive responses of wild populations to selection.

Evolutionary allometry reveals a shift in selection pressure on male horn size.

How selection pressures acting within species interact with developmental constraints to shape macro-evolutionary patterns of species divergence is still poorly understood. In particular, whether or not sexual selection affects evolutionary allometry, the increase in trait size with body size across species, of secondary sexual characters, remains largely unknown. In this context, bovid horn size is an especially relevant trait to study because horns are present in both sexes, but the intensity of sexual selection acting on them is expected to vary both among species and between sexes. Using a unique data set of sex-specific horn size and body mass including 91 species of bovids, we compared the evolutionary allometry between horn size and body mass between sexes while accounting for both the intensity of sexual selection and phylogenetic relationship among species. We found a nonlinear evolutionary allometry where the allometric slope decreased with increasing species body mass. This pattern, much more pronounced in males than in females, suggests either that horn size is limited by some constraints in the largest bovids or is no longer the direct target of sexual selection in very large species.

When relative allocation depends on total resource acquisition: implication for the analysis of trade-offs.

A central tenet of evolutionary biology states that life-history traits are linked via trade-offs, as classically exemplified by the van Noordwijk and de Jong model. This model, however, assumes that the relative resource allocation to a biological function varies independently of the total resource acquisition. Based on current empirical evidence, we first explored the dependency between the total resource acquisition and the relative resource allocation to reproduction and showed that such dependency is the rule rather than the exception. We then derived the expression of the covariance between traits when the assumption of independence is relaxed and used simulations to quantify the importance of such dependency on the detection of trade-offs between current reproduction and future survival. We found that the dependency between the total energy acquisition and the relative allocation to reproduction can influence the probability to detect trade-offs between survival and reproduction. As a general rule, a negative dependency between the total energy acquisition and the relative allocation to reproduction should lead to a higher probability of detecting a trade-off in species with a fast pace of life, whereas a positive dependency should lead to a higher probability of detecting a trade-off in species with a slow pace of life. In addition to confirming the importance of resource variation to reveal trade-offs, our finding demonstrates that the covariance between resource allocation and resource acquisition is generally not null and also plays a fundamental role in the detection of trade-offs.

The link between behavioural type and natal dispersal propensity reveals a dispersal syndrome in a large herbivore.

When individuals disperse, they modify the physical and social composition of their reproductive environment, potentially impacting their fitness. The choice an individual makes between dispersal and philopatry is thus critical, hence a better understanding of the mechanisms involved in the decision to leave the natal area is crucial. We explored how combinations of behavioural (exploration, mobility, activity and stress response) and morphological (body mass) traits measured prior to dispersal were linked to the subsequent dispersal decision in 77 roe deer Capreolus capreolus fawns. Using an unusually detailed multi-trait approach, we identified two independent behavioural continuums related to dispersal. First, a continuum of energetic expenditure contrasted individuals of low mobility, low variability in head activity and low body temperature with those that displayed opposite traits. Second, a continuum of neophobia contrasted individuals that explored more prior to dispersal and were more tolerant of capture with those that displayed opposite traits. While accounting for possible confounding effects of condition-dependence (body mass), we showed that future dispersers were less neophobic and had higher energetic budgets than future philopatric individuals, providing strong support for a dispersal syndrome in this species.

Haematological parameters do senesce in the wild: evidence from different populations of a long-lived mammal.

Increasing evidence of senescence has been reported from long-term studies of wild populations. However, most studies have focused on life-history traits like survival, reproduction or body mass, generally from a single intensively monitored population. However, variation in the intensity of senescence across populations, and to a lesser extent between sexes, is still poorly understood. In addition, the pattern of age-specific changes in haematological parameters remains virtually unknown to date for any population of vertebrate living in the wild. Using repeated blood samples collected from known-aged (2-15 years of age) roe deer (Capreolus capreolus) from two populations facing highly different environmental conditions, we filled the gap. In particular, we investigated age-specific changes in haematocrit, albumin and creatinine. We reported clear evidence of senescence in all haematological parameters. Moreover, senescence patterns differed between sexes and populations. The rate of senescence was higher in males than in females for haematocrit with no site difference. On the other hand, the rate of senescence in creatinine was higher at Trois Fontaines than at Chizé with no sex difference. Our findings provide a first demonstration of age-specific declines in haematological parameters in wild populations of large herbivores and show that the process of senescence in vertebrates is not restricted to body mass or fitness components. We also demonstrate that the senescence pattern of haematological parameters is context dependent and varies both between sexes and according to environmental conditions.

The allometry between secondary sexual traits and body size is nonlinear among cervids.

Allometric relationships between sexually selected traits and body size have been extensively studied in recent decades. While sexually selected traits generally display positive allometry, a few recent reports have suggested that allometric relationships are not always linear. In male cervids, having both long antlers and large size provides benefits in terms of increased mating success. However, such attributes are costly to grow and maintain, and these costs might constrain antler length from increasing at the same rate as body mass in larger species if the quantity of energy that males can extract from their environment is limiting. We tested for possible nonlinearity in the relationship between antler size and body mass (on a log-log scale) among 31 cervids and found clear deviation from linearity in the allometry of antler length. Antler length increased linearly until a male body mass threshold at approximately 110 kg. Beyond this threshold, antler length did not change with increasing mass. We discuss this evidence of nonlinear allometry in the light of life-history theory and stress the importance of testing for nonlinearity when studying allometric relationships.

Modeling reproductive trajectories of roe deer females: fixed or dynamic heterogeneity?

The relative role of dynamic and fixed heterogeneity in shaping the individual heterogeneity observed in most life-history traits remains difficult to quantify. In a recent work, Tuljapurkar et al. (2009) suggested modeling individual heterogeneity in lifetime reproductive success by a null model building reproductive trajectories from a first-order Markov chain. According to this model, among-individual differences in reproductive trajectories would be generated by the stochastic transitions among reproductive states (such as breeder and non-breeder) due to dynamic heterogeneity. In this work, we analyze the individual variation in three reproductive metrics (reproductive status, fecundity, and reproductive success) in two populations of roe deer intensively monitored using Tuljapurkar et al. (2009)'s dynamic model. Moreover, we challenge the Tuljapurkar model previously used as a biological null model to test whether the observed distribution of reproductive success over the lifetime was generated by a stochastic process by modifying two steps of the previous model to build a full stochastic model. We show that a distribution generated by the full dynamic model proposed by Tuljapurkar et al. (2009) can be consistently interpreted as only generated from a stochastic biological process provided that the probabilities of transition among reproductive states used are independent of the current reproductive state and that the positive covariation that usually occurs between survival and reproduction among individuals is removed. Only the reproductive status of roe deer females could be restricted to a stochastic process described by the full stochastic model, probably because most females (>90%) were breeders in a given year. The fecundity of roe deer females could not be adequately described by the full dynamic and full stochastic model, and the observed distribution of female reproductive success differed from the one generated by a full dynamic model in which each individual reproductive trajectory was independent of the individual lifespan (second step of the full dynamic model changed). While there was clear evidence that dynamic heterogeneity occurred and accounted for a large part of the observed among-individual variation in reproductive trajectories of roe deer females, a stochastic process did not provide a suitable model for all reproductive metrics. Consequently, models including additional fixed and dynamic traits need to be built in order to separate the relative role of fixed and dynamic heterogeneities in generating reproductive trajectories.

Contrasted patterns of age-specific reproduction in long-lived seabirds.

While the number of studies providing evidence of actuarial senescence is increasing, and covers a wide range of taxa, the process of reproductive senescence remains poorly understood. In fact, quite high reproductive output until the last years of life has been reported in several vertebrate species, so that whether or not reproductive senescence is widespread remains unknown. We compared age-specific changes of reproductive parameters between two closely related species of long-lived seabirds: the small-sized snow petrel Pagodroma nivea, and the medium-sized southern fulmar Fulmarus glacialoides. Both are sympatric in Antarctica. We used an exceptional dataset collected over more than 40 years to assess age-specific variations of both breeding probability and breeding success. We found contrasted age-specific reproductive patterns between the two species. Reproductive senescence clearly occurred from 21 years of age onwards in the southern fulmar, in both breeding probability and success, whereas we did not report any decline in the breeding success of the snow petrel, although a very late decrease in the proportion of breeders occurred at 34 years. Such a contrasted age-specific reproductive pattern was rather unexpected. Differences in life history including size or migratory behaviour are the most likely candidates to account for the difference we reported in reproductive senescence between these sympatric seabird species.

Population density and sex do not influence fine-scale natal dispersal in roe deer.

It is commonly assumed that the propensity to disperse and the dispersal distance of mammals should increase with increasing density and be greater among males than among females. However, most empirical evidence, especially on large mammals, has focused on highly polygynous and dimorphic species displaying female-defence mating tactics. We tested these predictions on roe deer, a weakly polygynous species of large herbivore exhibiting a resource-defence mating tactic at a fine spatial scale. Using three long-term studies of populations that were subject to the experimental manipulation of size, we did not find any support for either prediction, whether in terms of dispersal probability or dispersal distance. Our findings of similar dispersal patterns in both sexes of roe deer suggest that the underlying cause of natal dispersal is not related to inbreeding avoidance in this species. The absence of positive density dependence in fine-scale dispersal behaviour suggests that roe deer natal dispersal is a pre-saturation process that is shaped by heterogeneities in habitat quality rather than by density per se.

Lifetime reproductive success and composition of the home range in a large herbivore.

The relationship between individual performance and nonrandom use of habitat is fundamental to ecology; however, empirical tests of this relationship remain limited, especially for higher orders of selection like that of the home range. We quantified the association between lifetime reproductive success (LRS) and variables describing lifetime home ranges during the period of maternal care (spring to autumn) for 77 female roe deer (Capreolus capreolus) at Trois-Fontaines, Champagne-Ardenne, France (1976-2000). We maintained population growth rate (adjusted to account for removals of non-focal animals) near rmax, which enabled us to define the fitness-habitat relationship in the absence of density effects. Using a negative binomial model, we showed that a roe deer's incorporation into its home range of habitat components important to food, cover, and edge (meadows, thickets, and increased density of road allowances) was significantly related to LRS. Further, LRS decreased with increasing age of naturally reclaimed meadows at the time of a deer's birth, which may have reflected a cohort effect related to, but not entirely explained by, a decline in quality of meadows through time. Predictive capacity of the selected model, estimated as the median correlation (rs) between predicted and observed LRS among deer of cross-validation samples, was 0.55. The strength of this relationship suggests that processes like selection of the site of a home range during dispersal may play a more important role in determining fitness of individuals than previously thought. Individual fitness of highly sedentary income breeders with high reproductive output such as roe deer should be more dependent on home range quality during the period of maternal care compared to capital breeders with low reproductive output. Identification of the most important habitat attributes to survival and reproduction at low density (low levels of intraspecific competition) may prove useful for defining habitat value ("intrinsic habitat value").

Immunosenescence patterns differ between populations but not between sexes in a long-lived mammal.

In animals, physiological mechanisms underlying reproductive and actuarial senescence remain poorly understood. Immunosenescence, the decline in the ability to display an efficient immune response with increasing age, is likely to influence both reproductive and actuarial senescence through increased risk of disease. Evidence for such a link has been reported from laboratory animal models but has been poorly investigated in the wild, where variation in resource acquisitions usually drives life-history trade-offs. We investigated immunosenescence patterns over 7 years in both sexes of two contrasting roe deer populations (Capreolus capreolus). We first measured twelve immune markers to obtain a thorough identification of innate and adaptive components of immunity and assessed, from the same individuals, the age-dependent variation observed in parasitic infections. Although the level of innate traits was maintained at old age, the functional innate immune traits declined with increasing age in one of two populations. In both populations, the production of inflammatory markers increased with advancing age. Finally, the adaptive response declined in late adulthood. The increasing parasite burden with age we reported suggests the effective existence of immunosenescence. Age-specific patterns differed between populations but not between sexes, which indicate that habitat quality could shape age-dependent immune phenotype in the wild.

Estimating individual contributions to population growth: evolutionary fitness in ecological time.

Ecological and evolutionary change is generated by variation in individual performance. Biologists have consequently long been interested in decomposing change measured at the population level into contributions from individuals, the traits they express and the alleles they carry. We present a novel method of estimating individual contributions to population growth and changes in distributions of quantitative traits and alleles. An individual's contribution to population growth is an individual's realized annual fitness. We demonstrate how the quantities we develop can be used to address a range of empirical questions, and provide an application to a detailed dataset of Soay sheep. The approach provides results that are consistent with those obtained using lifetime estimates of individual performance, yet is substantially more powerful as it allows lifetime performance to be decomposed into annual survival and fecundity contributions.

Platelet phosphoinositide signaling system: an overstimulated pathway in depression.

In order to test a possible depression-associated defect in signal transduction, platelet alpha 2-adrenergic-mediated phosphoinositide (PI) hydrolysis was measured, both in drug-free major depressed patients and in control healthy subjects. Results that express phospholipase C activity have shown significant increase in the metabolites of epinephrine-stimulated tritiated phosphatidyl-4,5-biphosphate (3H-PIP2) with respect to basal activity (saline-stimulated). Thrombin (2 units) and 10 mM sodium fluoride (NaF) also induced an increase in 3H-PIP2 metabolites. These increases were potentiated in drug-free depressed patients both in epinephrine-and thrombin-stimulated platelets. In contrast, sodium fluoride, which directly stimulates G protein without receptor interaction, did not differentiate between patients and controls with respect to PI hydrolysis. This result suggests a possible depression-associated defect in heterologous receptor-G protein interaction.

Platelet serotonin and plasma tryptophan in depressed patients: effect of drug treatment and clinical outcome.

Platelet serotonin and plasma tryptophan were studied in healthy subjects and in depressed patients before and during their antidepressant drug treatment. Before treatment, mean platelet serotonin level was normal in depressed patients compared with healthy subjects while a significant decrease in patients' plasma TRP was noted (t = 6.0, p < .001). The concentrations of platelet 5-HT level did not correlate with either plasma TRP or with clinical variables, that is, AMDP depression and AMDP anxiety scores. Antidepressant drugs treatment decreased platelet 5-HT level (ANOVA F = 8.27, p < .001) whatever the clinical outcome of the patient, whereas the changes observed in plasma TRP were positively related to the mood state change. These results suggest that platelet serotonin could be a good pharmacological model but has no relevance concerning the mood state.

Hypnotic action of flunitrazepam in the rat: does 5-HT mechanism play a role?

This study examined whether pharmacological manipulation of serotonergic (5-HT) systems would affect the hypnotic action of flunitrazepam in rats. Flunitrazepam, a potent hypnotic, was used alone or combined with parachlorophenylalanine (pCPA), an inhibitor of the synthesis of 5-HT, 8-OH-DPAT, a 5-HT1A receptor agonist and fluvoxamine, an inhibitor of the reuptake of 5-HT. Flunitrazepam increased the amount of orthodox sleep, the latency of rapid eye movement (REM) sleep and decreased the amount of REM sleep. The drug pCPA decreased the total sleep time and the amount of orthodox and REM sleep. Administration of flunitrazepam to pCPA-pretreated rats induced orthodox sleep in an identical way to that found in the controls. The drug 8-OH-DPAT increased wakefulness and the latency of REM sleep. The association of flunitrazepam with 8-OH-DPAT abolished the increase in waking seen after 8-OH-DPAT alone. In contrast, the combined treatment with flunitrazepam and 8-OH-DPAT resulted in a lengthening of the latency of REM sleep significantly greater than that observed with the same dose of each drug alone. Fluvoxamine increased the latency a decrease the amount of REM sleep. The association of fluvoxamine with flunitrazepam induced a decrease in REM sleep, equal to the sum of the effects of the two drugs alone. Fluvoxamine did not modify the other effects of flunitrazepam. The present experiments demonstrate that the association of pCPA, 8-OH-DPAT and fluvoxamine, did not alter the hypnogenic effect of flunitrazepam. The possibility of an involvement of 5-HT mechanisms in the effect of flunitrazepam on the phasic events in sleep is questionable.

Body mass and individual fitness in female ungulates: bigger is not always better.

In female vertebrates, differences in fitness often correspond to differences in phenotypic quality, suggesting that larger females have greater fitness. Variation in individual fitness can result from variation in life span and/or variation in yearly reproductive success, but no study has yet assessed the relationships between the components of fitness and phenotypic quality while controlling for life span. We tried to fill this gap using data from long-term monitoring (23 years) of marked roe deer and bighorn sheep, two ungulates with very different life histories. In both species, we found a strong positive relationship between an adult female's mass and her probability of reaching old age: over the long term, bigger is indeed better for ungulate females. On the other hand, we found no evidence in either species that heavier females had higher fitness when differences in life span were accounted for: over the short term, bigger is not necessarily better. Our results indicate that, while broad differences in phenotypic quality affect individual fitness, when differences in life span are accounted for phenotypic quality has no residual effect on fitness. Therefore, within a given range of phenotypic quality, bigger is not always better, for reasons which may differ between species.

Variation in growth form and precocity at birth in eutherian mammals.

Using the flexible Chapman-Richards model for describing the growth curves from birth to adulthood of 69 species of eutherian mammals, we demonstrate that growth form differs among eutherian mammals. Thereby the commonly used Gompertz model can no longer be considered as the general model for describing mammalian growth. Precocial mammals have their peak growth rate earlier in the growth process than altricial mammals. However, the position on the altricial-precocial continuum accounts for most growth-form differences only between mammalian lineages. Within mammalian genera differences in growth form are not related to precocity at birth. This indicates that growth form may have been associated with precocity at birth early in mammalian evolution, when broad patterns of body development radiated. We discuss four non-exclusive interpretations to account for the role of precocity at birth on the observed variation in growth form among mammals. Precocial and altricial mammals could differ according to (i) the distribution of energy output by the mother, (ii) the ability of the young to assimilate the milk yield, (iii) the allocation of energy by the young between competing functions and (iv) the position of birth between conception and attainment of physical maturity.