Sexes in sync: phenotypic plasticity, sexual selection and phenological synchrony between the sexes in a wild hibernator.

Desynchrony of phenological responses to climate change is a major concern for ecological communities. Potential uncoupling between one of the most fundamental divisions within populations, males and females, has not been well studied. To address this gap, we examined sex-specific plasticity in hibernation phenology in two populations of Columbian ground squirrels (Urocitellus columbianus). We find that both sexes display similar phenological plasticity to spring snowmelt dates in their timing of torpor termination and behavioural emergence from hibernation. As a result of this plasticity, the degree of protandry (i.e. males' emergences from hibernation preceding those of females) did not change significantly over the 27-year study. Earlier male behavioural emergence, relative to females, improved the likelihood of securing a breeding territory and increased annual reproductive success. Sexual selection favouring earlier male emergence from hibernation may maintain protandry in this population, but did not contribute to further advances in male phenology. Together, our results provide evidence that the sexes should remain synchronized, at least in response to the weather variation investigated here, and further support the role of sexual selection in the evolution of protandry in sexually reproducing organisms.

Guides and cheats: producer-scrounger dynamics in the human-honeyguide mutualism.

Foraging animals commonly choose whether to find new food (as 'producers') or scavenge from others (as 'scroungers'), and this decision has ecological and evolutionary consequences. Understanding these tactic decisions is particularly vital for naturally occurring producer-scrounger systems of economic importance, because they determine the system's productivity and resilience. Here, we investigate how individuals' traits predict tactic decisions, and the consistency and pay-offs of these decisions, in the remarkable mutualism between humans (Homo sapiens) and greater honeyguides (Indicator indicator). Honeyguides can either guide people to bees' nests and eat the resulting beeswax (producing), or scavenge beeswax (scrounging). Our results suggest that honeyguides flexibly switched tactics, and that guiding yielded greater access to the beeswax. Birds with longer tarsi scrounged more, perhaps because they are more competitive. The lightest females rarely guided, possibly to avoid aggression, or because genetic matrilines may affect female body mass and behaviour in this species. Overall, aspects of this producer-scrounger system probably increase the productivity and resilience of the associated human-honeyguide mutualism, because the pay-offs incentivize producing, and tactic-switching increases the pool of potential producers. Broadly, our findings suggest that even where tactic-switching is prevalent and producing yields greater pay-offs, certain phenotypes may be predisposed to one tactic.

Effects of heat waves on telomere dynamics and parental brooding effort in nestlings of the zebra finch (Taeniopygia castanotis) transitioning from ectothermy to endothermy.

Heat waves are predicted to be detrimental for organismal physiology with costs for survival that could be reflected in markers of biological state such as telomeres. Changes in early life telomere dynamics driven by thermal stress are of particular interest during the early post-natal stages of altricial birds because nestlings quickly shift from being ectothermic to endothermic after hatching. Telomeres of ectothermic and endothermic organisms respond differently to environmental temperature, but few investigations within species that transition from ectothermy to endothermy are available. Also, ambient temperature influences parental brooding behaviour, which will alter the temperature experienced by offspring and thereby, potentially, their telomeres. We exposed zebra finch nestlings to experimental heat waves and compared their telomere dynamics to that of a control group at 5, 12 and 80 days of age that encapsulate the transition from the ectothermic to the endothermic thermoregulatory stage; we also recorded parental brooding, offspring sex, mass, growth rates, brood size and hatch order. Nestling mass showed an inverse relationship with telomere length, and nestlings exposed to heat waves showed lower telomere attrition during their first 12 days of life (ectothermic stage) compared to controls. Additionally, parents of heated broods reduced the time they spent brooding offspring (at 5 days old) compared to controls. Our results indicate that the effect of heat waves on telomere dynamics likely varies depending on age and thermoregulatory stage of the offspring in combination with parental brooding behaviour during growth.

Associations between DNA methylation and telomere length during early life: Insight from wild zebra finches (Taeniopygia guttata).

Telomere length and DNA methylation (DNAm) are two promising biomarkers of biological age. Environmental factors and life history traits are known to affect variation in both these biomarkers, especially during early life, yet surprisingly little is known about their reciprocal association, especially in natural populations. Here, we explore how variation in DNAm, growth rate, and early-life conditions are associated with telomere length changes during development. We tested these associations by collecting data from wild, nestling zebra finches in the Australian desert. We found that increases in the level of DNAm were negatively correlated with telomere length changes across early life. We also confirm previously documented effects of post hatch growth rate and clutch size on telomere length in a natural ecological context for a species that has been extensively studied in the laboratory. However, we did not detect any effect of ambient temperature during developmental on telomere length dynamics. We also found that the absolute telomere length of wild zebra finches, measured using the in-gel TRF method, was similar to that of captive birds. Our findings highlight exciting new opportunities to link and disentangle potential relationships between DNA based biomarkers of ageing, and of physiological reactions to environmental change.

Maternal programming of offspring in relation to food availability in an insect (Forficula auricularia).

Maternal effects can induce adjustments in offspring phenotype to the environment experienced by the mother. Of particular interest is if mothers can programme their offspring to cope best under matching environmental conditions, but the evidence for such anticipatory maternal effects (AME) is limited. In this study, we manipulated experimentally the food availability experienced by mothers and their offspring in the European earwig (Forficula auricularia). Offspring produced by females that had access to high or low food quantities were cross-fostered to foster mothers experiencing matched or mismatched environments. Offspring experiencing food availability matching the one of their mothers had an increased survival to adulthood compared with offspring experiencing mismatched conditions. Females experiencing high food laid larger clutches. This clutch-size adjustment statistically explained the matching effect when offspring experienced high food, but not when experiencing low food conditions. There were no effects of matching on offspring growth and developmental rate. Overall, our study demonstrates that AME occurs in relation to food availability enhancing offspring survival to adulthood under matching food conditions.

Female partner preferences enhance offspring ability to survive an infection.

BACKGROUND: It is often suggested that mate choice enhances offspring immune resistance to infectious diseases. To test this hypothesis, we conducted a study with wild-derived house mice (Mus musculus musculus) in which females were experimentally mated either with their preferred or non-preferred male, and their offspring were infected with a mouse pathogen, Salmonella enterica (serovar Typhimurium). RESULTS: We found that offspring sired by preferred males were significantly more likely to survive the experimental infection compared to those sired by non-preferred males. We found no significant differences in the pathogen clearance or infection dynamics between the infected mice, suggesting that offspring from preferred males were better able to cope with infection and had improved tolerance rather than immune resistance. CONCLUSION: Our results provide the first direct experimental evidence within a single study that partner preferences enhance offspring resistance to infectious diseases.

Ectoparasites and fitness of female Columbian ground squirrels.

Parasites play an important role in the evolution of host traits via natural selection, coevolution and sexually selected ornaments used in mate choice. These evolutionary scenarios assume fitness costs for hosts. To test this assumption, we conducted an ectoparasite removal experiment in free-living Columbian ground squirrels (Urocittelus columbianus) in four populations over three years. Adult females were randomly chosen to be either experimentally treated with anti-parasite treatments (spot-on solution and flea powder, N = 61) or a sham treatment (control, N = 44). We expected that experimental females would show better body condition, increased reproductive success and enhanced survival. Contrary to our expectations, body mass was not significantly different between treatments at mating, birth of litter or weaning of young. Further, neither number nor size of young at weaning differed significantly between the two treatments. Survival to the next spring for adult females and juveniles was not significantly different between experimental and control treatments. Finally, annual fitness was not affected by the treatments. We concluded that females and their offspring were able compensate for the presence of ectoparasites, suggesting little or no fitness costs of parasites for females in the different colonies and during the years of our experiments.

Parent-offspring conflict and the genetic trade-offs shaping parental investment.

The genetic conflict between parents and their offspring is a cornerstone of kin selection theory and the gene-centred view of evolution, but whether it actually occurs in natural systems remains an open question. Conflict operates only if parenting is driven by genetic trade-offs between offspring performance and the parent's ability to raise additional offspring, and its expression critically depends on the shape of these trade-offs. Here we investigate the occurrence and nature of genetic conflict in an insect with maternal care, the earwig Forficula auricularia. Specifically, we test for a direct response to experimental selection on female future reproduction and correlated responses in current offspring survival, developmental rate and growth. The results demonstrate genetic trade-offs that differ in shape before and after hatching. Our study not only provides direct evidence for parent-offspring conflict but also highlights that conflict is not inevitable and critically depends on the genetic trade-offs shaping parental investment.

Multiple paternity does not depend on male genetic diversity.

Polyandry is common in many species and it has been suggested that females engage in multiple mating to increase the genetic diversity of their offspring (genetic diversity hypothesis). Multiple paternity occurs in 30% of litters in wild populations of house mice, Mus musculus musculus, and multiple-sired litters are genetically more diverse than single-sired ones. Here, we aimed to test whether female house mice produce multiple-sired litters when they have the opportunity to produce genetically diverse litters. We assessed the rates of multiple paternity when females could choose to mate with two males that were genetically dissimilar to each other (i.e. nonsiblings and MHC dissimilar) compared with when females could choose to mate with two males that were genetically similar to each other (i.e. siblings and shared MHC alleles). Multiple mating may depend upon a female's own condition, and, therefore, we also tested whether inbred (from full-sibling matings) females were more likely to produce multiple-sired progeny than outbred controls. Overall we found that 29% of litters had multiple sires, but we found no evidence that females were more likely to produce multiple-sired litters when they had the opportunity to mate with genetically dissimilar males compared with controls, regardless of whether females were inbred or outbred. Thus, our findings do not support the idea that female mice increase multiple paternity when they have the opportunity to increase the genetic diversity of their offspring, as expected from the genetic diversity hypothesis.

Scent marking increases male reproductive success in wild house mice.

Scent marking is often assumed to be a secondary sexual trait that increases males' mating and reproductive success, although direct evidence for this hypothesis is lacking. We conducted a study with wild-derived house mice, Mus musculus musculus, to test whether scent marking increases males' reproductive success when females can freely choose between two territorial males. We also experimentally manipulated males' competitive scent marking by exchanging scent-marked tiles between the neighbouring males' territories (intrusion treatment) or relocating males' tiles within their own territory (control). Experimental animals were tested twice and we examined whether individual males were consistent in their marking. We found that males marked more in the intrusion treatment than controls and more at shared territorial borders than elsewhere. We found high day-to-day variation in most individuals' scent marking, and yet the sum of individuals' scent marking was consistent over time and across different social conditions. Genetic paternity analyses revealed that males' scent marking significantly increased their reproductive success in both the intrusion treatment and the controls. Surprisingly, however, female social preference was not positively correlated with male scent marking. These results provide direct evidence that scent marking increases males' reproductive success when females can choose their mates, even though it did not increase females' social preferences.

Why do female mice mate with multiple males?

Females often show multi-male mating (MMM), but the adaptive functions are unclear. We tested whether female house mice (Mus musculus musculus) show MMM when they can choose their mates without male coercion. We released 32 females into separate enclosures where they could choose to mate with two neighboring males that were restricted to their own territories. We also tested whether females increase MMM when the available males appeared unable to exclude intruders from their territories. To manipulate territorial intrusion, we introduced scent-marked tiles from the neighboring males into males' territories, or we rearranged tiles within males' own territories as a control. Each female was tested in treatment and control conditions and we conducted paternity analyses on the 57 litters produced. We found that 46 % of litters were multiply sired, indicating that multiple paternity is common when females can choose their mates. Intrusion did not increase multiple paternity, though multiple paternity was significantly greater in the first trial when the males were virgins compared to the second trial. Since virgin male mice are highly infanticidal, this finding is consistent with the infanticide avoidance hypothesis. We also found that multiple paternity was higher when competing males showed small differences in their amount of scent marking, suggesting that females reduce MMM when they can detect differences in males' quality. Finally, multiple paternity was associated with increased litter size but only in the intrusion treatment, which suggests that the effect of multiple paternity on offspring number is dependent on male-male interactions.

Sexing the Sciuridae: a simple and accurate set of molecular methods to determine sex in tree squirrels, ground squirrels and marmots.

We determined the sequence of the male-specific minor histocompatibility complex antigen (Smcy) from the Y chromosome of seven squirrel species (Sciuridae, Rodentia). Based on conserved regions inside the Smcy intron sequence, we designed PCR primers for sex determination in these species that can be co-amplified with nuclear loci as controls. PCR co-amplification yields two products for males and one for females that are easily visualized as bands by agarose gel electrophoresis. Our method provides simple and reliable sex determination across a wide range of squirrel species.