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Nichols, H. J.

Publications and source records attributed to Nichols, H. J..

8 recordsLinked to original sources

Banded mongooses discriminate relatedness and MHC diversity in unfamiliar conspecifics

Olfactory cues are critical in mammalian social communication, conveying fitness-relevant information such as relatedness, genetic quality, and compatibility. Recognizing kin through scent can help avoid inbreeding depression and guide nepotistic behaviors, enhancing both direct and indirect fitness. While many species use familiarity to identify relatives, others rely on phenotype matching, where animals assess genetic similarity by comparing their own genetically determined odor with that of others. In banded mongooses, synchronized breeding disrupts familiarity cues, increasing reliance on alternative mechanisms for kin discrimination and mate selection. We tested whether banded mongooses use odors to assess genetic diversity and relatedness based on (1) major histocompatibility complex (MHC) genotypes and (2) neutral microsatellite loci that reflect genetic diversity and relatedness. We found that individuals respond differently to odors from unfamiliar individuals based on MHC diversity and genetic relatedness. Specifically, individuals show more interest in less MHC diverse and less related unfamiliar conspecifics, suggesting odor cues are used to evaluate threat level of intruders or competitors. Genetic diversity had no impact on responses to odors and was not significantly associated with MHC diversity, implying that responses to MHC diversity did not result from an underlying correlation with over-all genetic diversity. We also found no effect of MHC similarity, which might be caused by the limited sample size for this analysis. Our findings show that MHC diversity might signal the genetic quality of individuals, but regions of the genome other than MHC may be used to assess relatedness. These findings provide the basis for future research on the involvement of the MHC and other genes in social communication in species where phenotype matching is likely to be advantageous.

animal behavior and cognition↗

Sex-dependent influence of major histocompatibility complex diversity on fitness in a social mammal

Parasite infections affect males and females differently across a wide range of species, often due to differences in immune responses. Generally, females tend to have stronger immune defenses and lower parasite loads than males. The major histocompatibility complex (MHC) plays a crucial role in the adaptive immune response, and extensive research has explored how variation in this region influences infection and fitness outcomes. However, studies of sex-specific relationships between MHC variation and infection are scarce, perhaps because MHC genes are located on the autosomes, which are shared by both sexes. Here, we provide evidence of sexually antagonistic selection in a wild, group-living mammal--the banded mongoose. Using genetic and life history data collected from over 300 individuals across 25 years, we found that particularly MHC class I (MHC-I) but also MHC class II (MHC-II) diversity influence lifetime reproductive success differently in males and females. Specifically, higher MHC diversity is linked to increased fitness in males but decreased fitness in females. Furthermore, MHC diversity did not differ between the sexes, indicating an unresolved genetic sexual conflict. Our findings demonstrate that sexually antagonistic selection acts on the MHC and may operate across both MHC classes but differently. This study contributes to the growing body of evidence that sex is a significant factor in shaping host immunity and fitness.

evolutionary biology↗

Characterization of both major histocompatibility complex classes in a wild social mammal: the banded mongoose

The major histocompatibility complexs (MHC) role in the vertebrate adaptive immune response and its exceptional polymorphism make it a key target for studying adaptive gene evolution. However, previous studies on carnivore MHC have mostly focused on populations which experienced a severe bottleneck or are of general conservation concern. Hence, sample sizes are often small and generalizations about MHC diversity are unreliable. Furthermore, studies often focus on one MHC class and do not cover the whole peptide binding groove of the MHC molecule. Here, we characterize MHC class I (MHC-I) exon 2 and 3, encoding both the 1- and 2-domain of the MHC-I molecule, as well as MHC-II DRB exon 2 for a large sample (N = 282-485) of a wild mammal of least conservation concern, the banded mongoose. We found that MHC-I generally showed higher allelic diversity and polymorphism compared to MHC-II, which is in line with findings in humans that show higher diversifying selection acting on MHC-I. However, MHC-I exon 3 showed the lowest diversity, possibly due to its different role in generating the peptide binding groove of the class I molecule compared to exon 2. Moreover, we found selection to act more strongly on MHC-I exon 2 (domain 1) than exon 3 (domain 2). Despite frequent inbreeding, phylogenetic comparative analysis showed banded mongooses to have MHC diversity levels comparable with other carnivores of least concern. Phylogenetic analysis indicated a longer evolutionary trajectory for MHC-II compared to MHC-I as well as species-specific gene duplication of nonclassical sequences of MHC-I clustering with classical sequences. Trans-species polymorphism was detected for nonclassical MHC-I sequences suggesting homology or convergent evolution for these genes. Our study is the first to characterize both MHC classes of a social, wild carnivore using a high throughput sequencing approach with a large sample size and thereby provides the basis for further investigation of MHC structure and function within the banded mongoose and other carnivores.

genetics↗

Fitness incentives to male fighters undermine fighting performance in intergroup contests

In humans and other animal societies, groups engage in intergroup conflicts over resources. The success of groups in these conflicts depends on individual contributions to collective fighting, yet individuals may have personal fitness incentives to defect rather than fight, which could undermine group performance. Here we test the hypothesis that personal fitness incentives affect intergroup conflict success in wild banded mongooses (Mungos mungo). In this species, intergroup fights are sometimes initiated by estrous females, who gain outgroup matings while their male group-mates contribute most of the fighting effort. We found that group fighting success was highest when a groups females were in estrus, suggesting that, although females may initiate fights, their male group-mates seem motivated to chase away rival groups to defend their paternity. Surprisingly, we found that groups that won fights conceded more paternity to their rivals than groups that lost. In other words, behavioral "wins" did not always result in fitness "wins". Younger males were more successful at attaining paternity between groups compared to within their own groups, suggesting that they may forego intergroup fighting to focus on intergroup mating. Overall, our results suggest that personal fitness incentives--here, in the form of paternity--vary widely among group members and can undermine rather than promote collective fighting performance. Such conflicts of interest are likely inherent in group combat and can contribute to variation in the frequency and costliness of intergroup violence.

animal behavior and cognition↗

Strategic use of male alternative reproductive tactics in cooperatively breeding banded mongoose groups

Alternative reproductive tactics (ARTs) allow smaller or less competitive individuals to reproduce by avoiding direct fights through sneaky strategies. Within cooperatively breeding groups ARTs are rarely reported, potentially due to difficulties observing male reproductive behaviour in the wild, or reproductive suppression by fellow group members. In societies where all mating opportunities cannot be monopolised by one male, young males could use sneaky tactics as a stepping-stone to gain limited reproductive success while they grow in resource holding potential (RHP). Using 20 years of pedigree, weight, group demography, and behavioural data, we investigated the use of sneaky pesterer ARTs in wild banded mongooses. Instead of a stepping stone, pestering tactics were typically a rare back-up used by males displaced from mate guarding tactics by higher RHP rivals. Additionally, pesterers have lower siring success compared to mate guards, despite similar weight loss costs, which may explain why most males settle for reproductive inactivity rather than use pestering tactics. However, pestering allows younger males to gain access to older, higher fecundity females in the group and may even facilitate inbreeding avoidance. Overall, ARTs provide a viable option for reproductive fitness for some males that lose out on reproductive positions in highly male-skewed groups.

animal behavior and cognition↗

Where are the beachmasters? Unexpectedly weak polygyny among southern elephant seals on a South Shetland Island

Intraspecific variation in animal mating systems can have important implications for ecological, evolutionary and demographic processes in wild populations. For example, patterns of mating can impact social structure, dispersal, effective population size and inbreeding. However, few species have been studied in sufficient detail to elucidate mating system plasticity and its dependence on ecological and demographic factors. Southern elephant seals (Mirounga leonina) have long been regarded as a textbook example of a polygynous mating system, with dominant beachmaster males controlling harems of up to several hundred females. However, behavioural and genetic studies have uncovered appreciable geographic variation in the strength of polygyny among elephant seal populations. We therefore used molecular parentage analysis to investigate patterns of parentage in a small satellite colony of elephant seals at the South Shetland Islands. We hypothesised that dominant males would be able to successfully monopolise the relatively small numbers of females present in the colony, leading to relatively high levels of polygyny. A total of 424 individuals (comprising 33 adult males, 101 adult females and 290 pups) sampled over eight years were genotyped at 20 microsatellites and reproductive success was analysed by genetically assigning parents. Paternity could only be assigned to 31 out of 290 pups (10.7%), despite our panel of genetic markers being highly informative and the genotyping error rate being very low. The strength of inferred polygyny was weak in comparison to previous genetic studies of the same species, with the most successful male fathering only seven pups over the entire course of the study. Our results show that, even in a species long regarded as a model for extreme polygyny, male reproductive skew can vary substantially among populations.

animal behavior and cognition↗

Early sexual dimorphism in the developing gut microbiome of northern elephant seals

The gut microbiome is an integral part of a species ecology, but we know little about how host characteristics impact its development in wild populations. Here, we explored the role of such intrinsic factors in shaping the gut microbiome of northern elephant seals during a critical developmental window of six weeks after weaning, when the pups stay ashore without feeding. We show that the early-life gut microbiome is already substantially different in male and female pups, even though males and females cannot yet be distinguished morphologically. Sex and age both explain around 15% of the variation in gut microbial beta diversity, while microbial communities sampled from the same individual show high levels of similarity across time, explaining another 40% of the variation. Only a small proportion of the variation in beta diversity is explained by health status, but healthy individuals have a greater microbial alpha diversity than their non-healthy peers. Across the post-weaning period, the elephant seal gut microbiome is highly dynamic. We found evidence for several colonisation and extinction events as well as a decline in Bacteriodes and an increase in Prevotella, a pattern that has previously been associated with the transition from nursing to solid food. Lastly, we show that genetic relatedness is correlated with gut microbiome similarity in males but not females, again reflecting substantial early sex-differences. Our study represents a naturally diet-controlled and longitudinal investigation of how intrinsic factors shape the early gut microbiome in a species with extreme sex differences in morphology and life history.

molecular biology↗

Recent demographic histories and genetic diversity across pinnipeds are shaped by anthropogenic interactions and mediated by ecology and life-history

A central paradigm in conservation biology is that population bottlenecks reduce genetic diversity and negatively impact population viability and adaptive potential. In an era of unprecedented biodiversity loss and climate change, understanding both the determinants and consequences of bottlenecks in wild populations is therefore an increasingly important challenge. However, as most studies have focused on single species, the multitude of potential drivers and the consequences of bottlenecks remain elusive. Here, we used a comparative approach by integrating genetic data from over 11,000 individuals of 30 pinniped species with demographic, ecological and life history data to elucidate the consequences of large-scale commercial exploitation by 18th and 19th century sealers. We show that around one third of these species exhibit strong genetic signatures of recent population declines, with estimated bottleneck effective population sizes reflecting just a few tens of surviving individuals in the most extreme cases. Bottleneck strength was strongly associated with both breeding habitat and mating system variation, and together with global abundance explained a large proportion of the variation in genetic diversity across species. Overall, there was no relationship between bottleneck intensity and IUCN status, although three of the four most heavily bottlenecked species are currently endangered. Our study reveals an unforeseen interplay between anthropogenic exploitation, ecology, life history and demographic declines, sheds new light on the determinants of genetic diversity, and is consistent with the notion that both genetic and demographic factors influence population viability.

evolutionary biology↗