Alternative reproductive strategies provide a flexible mechanism for assuring mating success in the European badgers (Meles meles): An investigation from hormonal measures.

Selection-pressures differ with population density, but few studies investigate how this can affect reproductive physiology. European badger (Meles meles) density varies from solitary to group-living across their range, with reported mating periods throughout the entire year to specific seasonal periods. Badger reproduction is evolutionarily distinct, interrupting the direct progression from conception to gestation with delayed implantation (DI), allowing for superfecundation (SF). To establish the tactical mating flexibility afforded by DI*SF, we used cross-sectional population-level seasonal variation of circulating sex-steroids for 97 females from a high-density population. Oestradiol was highest in spring among non-parous females, then lower in summer, and remained low during following seasons, suggesting that the mating period was restricted to just spring. Oestrone was consistently higher than oestradiol; it was elevated in spring, lowest during summer, peaked in autumn, and remained elevated for pregnant females in winter. This suggests that oestrone sustains pre-implanted blastocysts throughout DI. Progesterone was low throughout, except during winter pregnancy, associated with implantation and luteal development. In contrast to multiple mating periods reported by lower-density studies, our oestradiol data suggest that, at high-density, females exhibit only one mating period (congruent with testosterone patterns in males studied previously in this same population). While additional mating periods during DI enhance fertility assurance at low-density, at high-density, we propose that when coitus is frequent, fertilisation is assured, precluding the need for further cycles and associated mating risks. This endocrinologically flexible DI*SF mating strategy likely represents a form of balancing selection, allowing badgers to succeed at a range of regional densities.

A non-invasive method to assess the reproductive status of the European badger (Meles meles) from urinary sex-steroid metabolites.

Due to their unique reproductive physiology and behaviour, European badgers (Meles meles) are often used as a model to study mammalian reproduction. For reproductive endocrinology, circulating hormone levels are conventionally measured directly from blood samples. However, routine blood sampling is often not practical for wild animals and may induce stress affecting measurement accuracy. Non-invasive alternatives are thus of interest. Circulating hormones are metabolized through different routes, either by the kidneys, to be excreted through urine, or by the liver, to be excreted through faeces. These metabolites can thus be used as a proxy of hormone measurements, provided the species-specific metabolic characteristics are known. Here we tested the suitability of measuring urinary metabolites of circulating plasma sex-steroid hormones (testosterone in males and oestrogen in females) with enzyme immunoassays to assess the reproductive status of the European badger (Meles meles). Biological validation evidenced that urinary testosterone metabolite (UTM) and urinary total oestrogen metabolite (UEM) excretion patterns both corresponded with seasonal badger reproductive patterns on a population level, signaling correlation over a broad time frame. On an individual level, concurrent sampling of urine and plasma showed that male plasma testosterone and UTM levels correlated significantly across seasons, but no short term correlation was evident for total oestrogen and UEM in females. Thus, in badgers, urinary sex-steroid metabolites can be used reliably in the short term to assess male reproductive status at the individual level, but only at the broader population level for females.

Reproductive and Somatic Senescence in the European Badger (Meles meles): Evidence from Lifetime Sex-Steroid Profiles.

Among the Carnivora, there is sparse evidence for any substantive fitness benefits of post reproductive lifespan (PRLS, survival after reproductive cessation, RC). Using the European badger (Meles meles) as a model species, we analyzed sex-specific cross-sectional endocrinological and morphological data to investigate: 1) age-dependent reproductive decline in sex-steroid levels versus prime reproductive age; 2) age-dependent declines in somatic condition and reproductive advertisement (from subcaudal scent gland secretion); 3) changes in reproductive success with age due to somatic and endocrinological decline; 4) occurrence of RC, PRLS, and post reproductive representation (PrR) in the population with reference to pre-pubescent hormone levels and evidenced by fewer cub assignments from pedigree. We provide strong evidence for a gradual, not abrupt, decline in sex-steroid levels with age, with both sexes following a concave (down) quadratic trend. For both sexes, the onset of decline in somatic condition commenced at the age of 3 years. In contrast, decline in reproductive hormones started at age ca. 5.5 years in females and 6 years in males, with similar rates of decline thereafter. Subcaudal gland secretion volume also decreased in both sexes, especially after age 5, suggesting less investment in reproductive advertisement. After age 3, fewer (surviving) females were assigned cubs. This coincided with the onset of somatic decline but came earlier than hormonal decline (5.5 years onwards). The decrease in offspring assignments commenced later in males at age 5-6 years; concomitant with onset of testosterone decline at 6 years. This suggests that, contrary to females, in males declining body condition does not preclude reproductive success (no 'restraint') in advance of hormonal senescence ('constraint'). There was evidence of female PRLS, with very old adults living up to 2.59 ± 1.29 years after RC; although in males this evidence was weaker. We discuss the implications of these findings for RC and PRLS in the context of adaptive and non-adaptive hypotheses. There was evidence of over 2 years of Post Reproductive Life Span in both sexes.

Heterochrony of puberty in the European badger (Meles meles) can be explained by growth rate and group-size: Evidence for two endocrinological phenotypes.

Puberty is a key stage in mammalian ontogeny, involving endocrinological, physiological and behavioural changes, moderated by intrinsic and extrinsic factors. Thus, not all individuals within one population achieve sexual maturity simultaneously. Here, using the European badger (Meles meles) as a model, we describe male testosterone and female oestrone profiles (using Enzyme-immunoassays) from first capture (3 months, post-weaning) until 28 months (attaining sexual maturity and final body size), along with metrics of somatic growth, scent gland development and maturation of external reproductive organs as well as intra-specific competition. In both sexes, endocrinological puberty commenced at ca. 11 months. Thereafter, cub hormone levels followed adult seasonal hormone patterns but at lower levels, with the majority of cubs reaching sexual maturity during their second mating season (22-28 months). Interestingly, there was evidence for two endocrinological phenotypes among male cubs (less evident in females), with early developers reaching sexual maturity at 11 months (first mating season) and late developers reaching sexual maturity at 22-26 months (second mating season). Early developers also attained a greater proportion of their ultimate adult size by 11 months, exhibiting faster growth rates than late developers (despite having similar adult size). Male cubs born into larger social groups tended to follow the late developer phenotype. Our results support the hypothesis that a minimum body size is required to reach sexual maturity, which may be achieved at different ages, even within a single population, where early maturity can confer individual fitness advantages and enhance population growth rate.