Ivermectin decreases parasite load, testosterone, and potentially antler length in a group of captive red deer males (Cervus elaphus).

Secondary sex traits (SSTs) can favour males in intra-sexual competition, allowing females to reliably assess their quality. They can also be connected to other aspects of fitness, such as resistance to parasites and pathogens, as parasites have negative effects on the development of SSTs. Antlers are one of the most recognizable examples of SSTs whose development is regulated by testosterone and reflects the actual condition of the bearer. Elevated testosterone can exaggerate the size of SSTs while impairing the function of the immune system ("The Immunocompetence Handicap Hypothesis") posing a trade-off between antler development and immune function. In this study, we experimentally manipulated the parasite load in captive red deer (Cervus elaphus) males with Ivermectin during antler development for two consecutive years. Expecting an inverse proportionality between parasite load and antler size, we hypothesized the treated deer to have larger antlers than the untreated ones. Our results showed that, following the immunocompetence handicap hypothesis, parasite load was positively associated with testosterone levels. However, the application of Ivermectin suppressed the parasite load of the treated animals but did not lead to the development of larger antlers. Instead, it significantly suppressed the concentration of testosterone in the treated animals, whilst the animals that had higher testosterone also had the highest parasite load. Our findings show that Ivermectin can potentially decrease the levels of testosterone and, consequently, antler size. These findings have important implications for the management of captive populations, especially in contexts where the development of large trophies is desired.

The effects of challenge or social buffering on cortisol, testosterone, and antler growth in captive red deer (Cervus elaphus) males.

We equipped 17 captive red deer males (Cervus elaphus) with GPS collars to measure inter-individual distances throughout the 5-months of the antler growth period. We expected some individuals to associate regularly with others while others would not. We predicted that males aggregating with others within a socially stable environment (Associates) would benefit from a form of "social buffering" and would likely have lowered cortisol (C) and testosterone (T) concentrations. Males only irregularly joining social groupings would experience elevated levels of aggression; according to the "Challenge hypothesis", their T and C concentrations should increase. Interacting with a higher proportion of Associates did indeed reduce C concentrations. Conversely, avoiding Associates and challenging other males stimulated the T secretion. Admittedly, males avoiding regular proximity to others tended to develop the largest antlers. They probably benefited from frequent successful agonistic threats to conspecifics, resulting in elevated T concentrations. Regular association with tolerant, conspecifics and "social buffering" did not seem sufficient for producing larger antlers despite reducing C concentrations. Alternative social strategies were adopted within the same group of individuals and showed how the trade-off between these strategies could have an essential impact on C and T concentrations.

To beat or not to beat: Behavioral plasticity during the antler growth period affects cortisol but not testosterone concentrations in red deer (Cervus elaphus) males.

Out of rut, male red deer (Cervus elaphus) associate themselves in bachelor groups where animals compete for rank position via agonistic interactions. In a previous study on red deer, males were recognized either as "Non-Fighters" (NF, low frequency of attacks) or "Fighters" (F, high frequency of attacks). This study, therefore, aims to verify the consistency of the inter-individual differences in fighting attitude across different social contexts and investigate whether they could be considered an individual characteristic. Behavioral consistency was presumed across three different sampling seasons, assuming that NF would have lower cortisol (C) and testosterone (T) concentrations than the F males. In 2015 the males were kept in one large group and labelled NF and F. In 2016, the herd was divided into two subgroups ("NF" and "F") based on the frequency of attacks. Finally, in 2017, the males were divided into two randomly composed subgroups. Data about agonistic behavior and concentration of C and T were collected during each season. In 2015 the individuals differed only for the fighting attitude. After the division, the frequency of the attacks always increased, being consistently lower in NF than in F. Unexpectedly, a slight increase in the concentration of C was detected in the NF in 2016, compared to the F who experienced no difference neither in 2015 nor 2017. No significant differences were found in T. We concluded that, even though the males had shown behavioral plasticity, their diversified interaction-prone attitude had been maintained despite the modifications of the social environment.

When the ball is in the female's court: How the scramble-competition mating system of the North American red squirrel has shaped male physiology and testosterone dynamics.

Male reproductive success in most mammals is determined by their success in direct inter-male competition through aggression and conflict, resulting in female-defense mating systems being predominant. This is linked to male testosterone levels and its dynamics. However, in certain environments, a scramble-competition mating system has evolved, where female reproductive behavior takes precedence and male testosterone dynamics are unlikely to be related to inter-male competition. We studied the North American red squirrel (Tamiasciurus hudsonicus), a species with a well-established scramble-competition system. Using an ACTH hormonal challenge protocol as a proxy for competitive interactions, we compared the testosterone dynamics in breeding males in late winter with that in nonbreeding males in late spring in the Yukon. To gain an integrated picture of their physiological state, we also assessed changes in their stress response, body mass, energy mobilization, and indices of immune function. Testosterone levels at the base bleed were high in breeding males (2.72ng/mL) and virtually absent in non-breeding males (0.04ng/mL). Breeding males were in better condition (heavier body mass, higher hematocrit, and higher erythrocytes), had higher indices of immune function (neutrophil:lymphocyte ratio), but a similar ability to mobilize energy (glucose) compared with non-breeding males. Though total cortisol was higher in non-breeding males, free cortisol was twice as high in breeding males as their corticosteroid binding globulin levels were half as high. In response to the ACTH challenge, testosterone levels in breeding males declined 49% over the first hour and increased 36% over the next hour; in non-breeding males levels showed no change. Free cortisol increased only modestly (26% in breeding males; 23% in non-breeding males). Glucose levels changed similarly in breeding and nonbreeding males, declining for the first 30min and then increasing for the next 60min. Thus, testosterone and components of the stress axis function in a profoundly different manner in male red squirrels than in males of mammals with female-defense mating systems. There are four probable interrelated reasons for these adaptations in male red squirrels: the marginal benefits of each mating, the constraints of mate searching away from their own resource-based territories, energy mobilization in a harsh environment, and a long life span.

Correction: Pre-breeding food restriction promotes the optimization of parental investment in house mice, Mus musculus.

[This corrects the article DOI: 10.1371/journal.pone.0173985.].

Pre-breeding food restriction promotes the optimization of parental investment in house mice, Mus musculus.

Litter size is one of the most reliable state-dependent life-history traits that indicate parental investment in polytocous (litter-bearing) mammals. The tendency to optimize litter size typically increases with decreasing availability of resources during the period of parental investment. To determine whether this tactic is also influenced by resource limitations prior to reproduction, we examined the effect of experimental, pre-breeding food restriction on the optimization of parental investment in lactating mice. First, we investigated the optimization of litter size in 65 experimental and 72 control families (mothers and their dependent offspring). Further, we evaluated pre-weaning offspring mortality, and the relationships between maternal and offspring condition (body weight), as well as offspring mortality, in 24 experimental and 19 control families with litter reduction (the death of one or more offspring). Assuming that pre-breeding food restriction would signal unpredictable food availability, we hypothesized that the optimization of parental investment would be more effective in the experimental rather than in the control mice. In comparison to the controls, the experimental mice produced larger litters and had a more selective (size-dependent) offspring mortality and thus lower litter reduction (the proportion of offspring deaths). Selective litter reduction helped the experimental mothers to maintain their own optimum condition, thereby improving the condition and, indirectly, the survival of their remaining offspring. Hence, pre-breeding resource limitations may have facilitated the mice to optimize their inclusive fitness. On the other hand, in the control females, the absence of environmental cues indicating a risky environment led to "maternal optimism" (overemphasizing good conditions at the time of breeding), which resulted in the production of litters of super-optimal size and consequently higher reproductive costs during lactation, including higher offspring mortality. Our study therefore provides the first evidence that pre-breeding food restriction promotes the optimization of parental investment, including offspring number and developmental success.

A sociobiological origin of pregnancy failure in domestic dogs.

Among domestic dog breeders it is common practice to transfer a domestic dog bitch out of her home environment for mating, bringing her back after the mating. If the home environment contains a male, who is not the father of the foetuses, there is a potential risk of future infanticide. We collected 621 records on mating of 249 healthy bitches of 11 breed-types. The highest proportion of successful pregnancies following mating occurred in bitches mated within their home pack and remaining there. Bitches mated elsewhere and then returned to a home containing at least one male had substantially lower incidence of maintained pregnancy in comparison with bitches mated by a home male. After returning home, housing affected strongly the frequency of pregnancy success. Bitches mated elsewhere but released into a home pack containing a home male were four times more likely to maintain pregnancy than bitches which were housed individually after returning home. Suppression of pregnancy in situations where a bitch is unable to confuse a home male about parentage may be seen as an adaptation to avoid any seemingly unavoidable future loss of her progeny to infanticide after birth and thus to save energy.

Developmental instability of ano-genital distance index: Implications for assessment of prenatal masculinization.

Prenatal androgens are generally assumed to permanently affect the morphology of external genitalia. In laboratory rodents, the ano-genital distance index (AGDI) has become widely used as a marker of natural prenatal masculinization. A greater value should indicate a greater masculinization. The aim of this study was to assess the developmental stability of the AGDI in female mice during pre- (Days 1-21) and postweaning (Days 21-61) periods. Presuming that the AGDI reflects a permanent effect of prenatal masculinization, we hypothesized that the AGDI will be a developmentally stable morphometric measurement (interindividual differences in the AGDI measurement should persist over time). In contrast to our prediction, the AGDI showed poor repeatability both during pre- (.15) and postweaning (.22) periods, indicating developmental instability. (A value of 1 indicates perfect repeatability and a value of 0 indicates no repeatability.) The AGDI thus does not seem to be a reliable marker of prenatal female masculinization.