Patterns of philopatry and longevity contribute to the evolution of post-reproductive lifespan in mammals

While menopause has long been known as a characteristic trait of human reproduction, evidence for post-reproductive lifespan (PRLS) has recently been found in other mammals. Adaptive and non-adaptive hypotheses have been proposed to explain the evolution of PRLS, but formal tests of these are rare. We use a phylogenetic approach to evaluate hypotheses for the evolution of PRLS among mammals. In contrast to theoretical models predicting that PRLS may be promoted by male philopatry (which increases relatedness between a female and her group in old age), we find little evidence that male philopatry led to the evolution of a post-reproductive period. However, the proportion of life spent post-reproductive was related to lifespan and patterns of philopatry, suggesting that the duration of PRLS may be impacted by both non-adaptive and adaptive processes. Finally, the proportion of females experiencing PRLS was higher in species with male philopaty and larger groups, in accordance with adaptive models of PRLS. We suggest that the origin of PRLS primarily follows the non-adaptive 'mismatch' scenario, but that patterns of philopatry may subsequently confer adaptive benefits of late-life helping

Evidence for frequent incest in a cooperatively breeding mammal.

As breeding between relatives often results in inbreeding depression, inbreeding avoidance is widespread in the animal kingdom. However, inbreeding avoidance may entail fitness costs. For example, dispersal away from relatives may reduce survival. How these conflicting selection pressures are resolved is challenging to investigate, but theoretical models predict that inbreeding should occur frequently in some systems. Despite this, few studies have found evidence of regular incest in mammals, even in social species where relatives are spatio-temporally clustered and opportunities for inbreeding frequently arise. We used genetic parentage assignments together with relatedness data to quantify inbreeding rates in a wild population of banded mongooses, a cooperatively breeding carnivore. We show that females regularly conceive to close relatives, including fathers and brothers. We suggest that the costs of inbreeding avoidance may sometimes outweigh the benefits, even in cooperatively breeding species where strong within-group incest avoidance is considered to be the norm

GCalignR: An R package for aligning gas-chromatography data for ecological and evolutionary studies.

Chemical cues are arguably the most fundamental means of animal communication and play an important role in mate choice and kin recognition. Consequently, there is growing interest in the use of gas chromatography (GC) to investigate the chemical basis of eco-evolutionary interactions. Both GC-MS (mass spectrometry) and FID (flame ionization detection) are commonly used to characterise the chemical composition of biological samples such as skin swabs. The resulting chromatograms comprise peaks that are separated according to their retention times and which represent different substances. Across chromatograms of different samples, homologous substances are expected to elute at similar retention times. However, random and often unavoidable experimental variation introduces noise, making the alignment of homologous peaks challenging, particularly with GC-FID data where mass spectral data are lacking. Here we present GCalignR, a user-friendly R package for aligning GC-FID data based on retention times. The package was developed specifically for ecological and evolutionary studies that seek to investigate similarity patterns across multiple and often highly variable biological samples, for example representing different sexes, age classes or reproductive stages. The package also implements dynamic visualisations to facilitate inspection and fine-tuning of the resulting alignments and can be integrated within a broader workflow in R to facilitate downstream multivariate analyses. We demonstrate an example workflow using empirical data from Antarctic fur seals and explore the impact of user-defined parameter values by calculating alignment error rates for multiple datasets. The resulting alignments had low error rates for most of the explored parameter space and we could also show that GCalignR performed equally well or better than other available software. We hope that GCalignR will help to simplify the processing of chemical datasets and improve the standardization and reproducibility of chemical analyses in studies of animal chemical communication and related fields

Kin discrimination via odour in the cooperatively breeding banded mongoose

Kin discrimination is often beneficial for group-living animals as it aids in inbreeding avoidance and providing nepotistic help. In mammals, the use of olfactory cues in kin discrimination is widespread and may occur through learning the scents of individuals that are likely to be relatives, or by assessing genetic relatedness directly through assessing odour similarity (phenotype matching). We use scent presentations to investigate these possibilities in a wild population of the banded mongoose Mungos mungo, a cooperative breeder in which inbreeding risk is high and females breed communally, disrupting behavioural cues to kinship. We find that adults show heightened behavioural responses to unfamiliar (extra-group) scents than to familiar (within-group) scents. Interestingly, we found that responses to familiar odours, but not unfamiliar odours, varied with relatedness. This suggests that banded mongooses are either able to use an effective behavioural rule to identify likely relatives from within their group, or that phenotype matching is used in the context of within-group kin recognition but not extra-group kin recognition. In other cooperative breeders, familiarity is used within the group and phenotype matching may be used to identify unfamiliar kin. However, for the banded mongoose this pattern may be reversed, most likely due to their unusual breeding system which disrupts within-group behavioural cues to kinship

inbreedR: An R package for the analysis of inbreeding based on genetic markers

1. Heterozygosity fitness correlations (HFCs) have been used extensively to explore the impact of inbreeding on individual fitness. Initially, most studies used small panels of microsatellites, but more recently with the advent of next generation sequencing, large SNP datasets are becoming increasingly available and these provide greater power and precision to quantify the impact of inbreeding on fitness. 2. Despite the popularity of HFC studies, effect sizes tend to be rather small. One reason for this may be a low variation in inbreeding level across individuals. Using genetic markers, it is possible to measure variance in inbreeding through the strength of correlation in heterozygosity across marker loci, termed identity disequilibrium (ID). 3. ID can be quantified using the measure g2 which is also a central parameter in HFC theory that can be used within a wider framework to estimate the direct impact of inbreeding on both marker heterozygosity and fitness. However, no software exists to calculate g2 for large SNP datasets nor to implement this framework. 4. inbreedR is an R package that provides functions to calculate g2 based on microsatellite and SNP markers with associated p-values and confidence intervals. Within the framework of HFC theory, inbreedR also estimates the impact of inbreeding on marker heterozygosity and fitness. Moreover, we implemented easy-to-use simulations to explore the precision and magnitude of estimates based on different numbers of genetic markers. We hope this package will facilitate good practice in the analysis of HFCs and help to deepen our understanding of inbreeding effects in natural populations

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively-breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicative of a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard-female relatedness did not affect the guard’s probability of gaining reproductive success. However, where mate-guards are unsuccessful they lose paternity to males that are less related to the females than themselves. Together our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited

Reproductive competition triggers mass eviction in cooperative banded mongooses

In many vertebrate societies, forced eviction of group members is an important determinant of population structure, but little is known about what triggers eviction. Three main explanations are (1) the reproductive competition hypothesis; (2) the coercion of cooperation hypothesis; and (3) the adaptive forced dispersal hypothesis. The last hypothesis proposes that dominant individuals use eviction as an adaptive strategy to propagate copies of their alleles through a highly structured population. We tested these hypotheses as explanations for eviction in cooperatively breeding banded mongooses (Mungos mungo), using a 16-year dataset on life history, behaviour and relatedness. In this species, groups of females, or mixed-sex groups, are periodically evicted en masse. Our evidence suggests that reproductive competition is the main ultimate trigger for eviction for both sexes. We find little evidence that mass eviction is used to coerce helping, or as a mechanism to force dispersal of relatives into the population. Eviction of females changes the landscape of reproductive competition for remaining males, which may explain why males are evicted alongside females. Our results show that the consequences of resolving within-group conflict resonate through groups and populations to affect population structure, with important implications for social evolution

Heterozygosity but not inbreeding coefficient predicts parasite burdens in the banded mongoose

This is the author accepted manuscript. The final version is available from Wiley via the DOI in this record.Inbreeding, reproduction between relatives, often impinges on the health and survival of resulting offspring. Such inbreeding depression may manifest itself through immunological costs as inbred individuals suffer increased propensity to disease, infection and parasites compared to outbred conspecifics. Here, we assess how the intestinal parasite loads of wild banded mongooses (Mungos mungo) vary with pedigree inbreeding coefficient (ƒ) and standardized multi-locus heterozygosity. We find a significant association between increased heterozygosity and lower parasite loads; however, this correlation does not stand when considering ƒ. Such findings may be explained by local genetic effects, linkage between genetic markers and genes influencing parasite burdens. Indeed, we find heterozygosity at certain loci to correlate with parasite load. Although these tentative local effects are lost following multiple test correction, they warrant future investigation to determine their strength and impact. We also suggest frequent inbreeding within banded mongooses may mean heterozygosity is a better predictor of inbreeding than pedigree ƒ. This is because inbreeding facilitates linkage disequilibrium, increasing the chances of neutral markers representing genome-wide heterozygosity. Finally, neither ƒ nor heterozygosity had a significant influence on the loads of two specific gastrointestinal parasites. Nevertheless, more heterozygous individuals benefited from reduced overall parasitic infection and genetic diversity appears to explain some variation in parasite burdens in the banded mongoose

Rat eradication comes within a whisker! A case study of a failed project from the South Pacific.

To enhance their conservation value, several hundred islands worldwide have been cleared of invasive alien rats, Rattus spp. One of the largest projects yet undertaken was on 43 km(2) Henderson Island in the Pitcairn group, South Pacific, in August 2011. Following massive immediate mortality, a single R. exulans was observed in March 2012 and, subsequently, rat numbers have recovered. The survivors show no sign of resistance to the toxicant used, brodifacoum. Using pre- and post-operation rat tissue samples from Henderson, plus samples from around the Pacific, we exclude re-introduction as the source of continued rat presence. Microsatellite analysis of 18 loci enabled comparison of genetic diversity of Henderson rats before and after the bait drop. The fall in diversity measured by allele frequency change indicated that the bottleneck (N e) through which the breeding population passed was probably around 50 individuals, representing a census population of about 60-80 animals. This is the first failed project that has estimated how close it was to success.The Darwin Initiative funded much of the RSPB’s work on Henderson Island and therefore sample collection and analysis, the latter also supported by the Sir Peter Scott Commemorative Expedition to the Pitcairn Islands

Female reproductive competition explains variation in prenatal investment in wild banded mongooses

Female intrasexual competition is intense in cooperatively breeding species where offspring compete locally for resources and helpers. In mammals, females have been proposed to adjust prenatal investment according to the intensity of competition in the postnatal environment (a form of ‘predictive adaptive response’; PAR). We carried out a test of this hypothesis using ultrasound scanning of wild female banded mongooses in Uganda. In this species multiple females give birth together to a communal litter, and all females breed regularly from one year old. Total prenatal investment (size times the number of fetuses) increased with the number of potential female breeders in the group. This relationship was driven by fetus size rather than number. The response to competition was particularly strong in low weight females and when ecological conditions were poor. Increased prenatal investment did not trade off against maternal survival. In fact we found the opposite relationship: females with greater levels of prenatal investment had elevated postnatal maternal survival. Our results support the hypothesis that mammalian prenatal development is responsive to the intensity of postnatal competition. Understanding whether these responses are adaptive requires information on the long-term consequences of prenatal investment for offspring fitness