Long term analysis of social structure: evidence of age-based consistent associations in Alpine ibex

ABSTRACTDespite its recognized importance for understanding the evolution of animal sociality as well as for conservation, long term analysis of social networks of animal populations is still relatively uncommon. We investigated social network dynamics in males of a gregarious mountain ungulate (Alpine ibex, Capra ibex) over ten years focusing on groups, sub-groups and individuals, exploring the dynamics of sociality over different scales. Despite the social structure changing between seasons, the Alpine ibex population was highly cohesive: fission-fusion dynamics lead almost every male in the population to associate with each other male at least once. Nevertheless, we found that male Alpine ibex showed preferential associations that were maintained across seasons and years. Age seemed to be the most important factor driving preferential associations while other characteristics, such as social status, appeared less crucial. We also found that centrality measures were influenced by age and were also related to individual physical condition. The multi-scale and long-term frame of our study helped us show that ecological constrains, such as resource availability, may play a role in shaping associations in a gregarious species, but they cannot solely explain sociality and preferential association that are likely also to be driven by life-history linked physiological and social needs. Our results highlight the importance of long-term studies based on individually recognizable subjects to help us build on our understanding of the evolution of animal sociality.

Ancient mitogenomes unravel massive genetic diversity loss during near extinction of Alpine ibex

Population bottlenecks can have dramatic consequences for the health and long-term survival of a species. A recent bottleneck event can also largely obscure our understanding of standing variation prior to the contraction. Historic population sizes can be modeled based on extant genomics, however uncertainty increases with the severity of the bottleneck. Integrating ancient genomes provides a powerful complement to retrace the evolution of genetic diversity through population fluctuations. Here, we recover 15 high-quality mitogenomes of the once nearly extinct Alpine ibex spanning 8601 BP to 1919 CE and combine these with 60 published modern genomes. Coalescent demography simulations based on modern genomes indicate population fluctuations matching major climatic change over the past millennia. Using ancient genomes, we show that mitochondrial haplotype diversity has been reduced to a fifth of the pre-bottleneck diversity with several highly differentiated mitochondrial lineages having co-existed historically. The main collapse of mitochondrial diversity coincided with human settlement expansions in the Middle Ages. The near extinction severely reduced the mitochondrial diversity. After recovery, one lineage was spread and nearly fixed across the Alps due to recolonization efforts. Contrary to expectations, we show that a second ancestral mitochondrial lineage has survived in an isolated population further south. Our study highlights that a combined approach integrating genomic data of ancient, historic and extant populations unravels major long-term population fluctuations.

Targeted strategies for the management of wildlife diseases: the case of brucellosis in Alpine ibex

The management of infectious diseases in wildlife reservoirs is challenging and faces several limitations. However, detailed knowledge of host–pathogen systems often reveal heterogeneity among the hosts’ contribution to transmission. Management strategies targeting specific classes of individuals and/or areas, having a particular role in transmission, could be more effective and more acceptable than population-wide interventions. In the wild population of Alpine ibex (Capra ibex—a protected species) of the Bargy massif (French Alps), females transmit brucellosis (Brucella melitensis) infection in ~90% of cases, and most transmissions occur in the central spatial units (“core area”). Therefore, we expanded an individual-based model, developed in a previous study, to test whether strategies targeting females or the core area, or both, would be more effective. We simulated the relative efficacy of realistic strategies for the studied population, combining test-and-remove (euthanasia of captured animals with seropositive test results) and partial culling of unmarked animals. Targeting females or the core area was more effective than untargeted management options, and strategies targeting both were even more effective. Interestingly, the number of ibex euthanized and culled in targeted strategies were lower than in untargeted ones, thus decreasing the conservation costs while increasing the sanitary benefits. Although there was no silver bullet for the management of brucellosis in the studied population, targeted strategies offered a wide range of promising refinements to classical sanitary measures. We therefore encourage to look for heterogeneity in other wildlife diseases and to evaluate potential strategies for improving management in terms of efficacy but also acceptability.

Limitations of using surrogates for behaviour classification of accelerometer data: refining methods using random forest models in Caprids

Background Animal-attached devices can be used on cryptic species to measure their movement and behaviour, enabling unprecedented insights into fundamental aspects of animal ecology and behaviour. However, direct observations of subjects are often still necessary to translate biologging data accurately into meaningful behaviours. As many elusive species cannot easily be observed in the wild, captive or domestic surrogates are typically used to calibrate data from devices. However, the utility of this approach remains equivocal. Methods Here, we assess the validity of using captive conspecifics, and phylogenetically-similar domesticated counterparts (surrogate species) for calibrating behaviour classification. Tri-axial accelerometers and tri-axial magnetometers were used with behavioural observations to build random forest models to predict the behaviours. We applied these methods using captive Alpine ibex (Capra ibex) and a domestic counterpart, pygmy goats (Capra aegagrus hircus), to predict the behaviour including terrain slope for locomotion behaviours of captive Alpine ibex. Results Behavioural classification of captive Alpine ibex and domestic pygmy goats was highly accurate (> 98%). Model performance was reduced when using data split per individual, i.e., classifying behaviour of individuals not used to train models (mean ± sd = 56.1 ± 11%). Behavioural classifications using domestic counterparts, i.e., pygmy goat observations to predict ibex behaviour, however, were not sufficient to predict all behaviours of a phylogenetically similar species accurately (> 55%). Conclusions We demonstrate methods to refine the use of random forest models to classify behaviours of both captive and free-living animal species. We suggest there are two main reasons for reduced accuracy when using a domestic counterpart to predict the behaviour of a wild species in captivity; domestication leading to morphological differences and the terrain of the environment in which the animals were observed. We also identify limitations when behaviour is predicted in individuals that are not used to train models. Our results demonstrate that biologging device calibration needs to be conducted using: (i) with similar conspecifics, and (ii) in an area where they can perform behaviours on terrain that reflects that of species in the wild.

Bronchopulmonary Nematodes in Alpine Ibex: Shedding of First Stage Larvae Analyzed at the Individual Host Level

Pneumonia is the most frequent cause of death for Alpine ibex (Capra ibex) in Gran Paradiso National Park, (Italy). The etiology of this form of pneumonia is currently unknown and the identification of the primary etiological agent remains difficult due to biological and logistic constraints. Uncovering individual differences in Protostrongylid prevalence and intensity is important to further investigate the epidemiology of respiratory diseases and their relationship to heterozygosity and inbreeding in a once almost extinct population like C. ibex. In a group of 21 individually recognizable adult male we monitored monthly prevalence and intensity of Protostrongylid first-stage larvae using Baerman's technique from June to September 2019. First-stage larvae of 5 genera were detected. Muellerius (P = 100%, CI95% = 84–100) and Protostrongylus (P = 86%, CI95%:71–100) were two dominant genera according to Bush's importance index. Neostrongylus (P = 38%,CI95%: 17–59), Cystocaulus (P = 33%,CI95% = 13–53) were classified as co-dominant genera while Dictyocaulus filaria (P = 0.05%, CI95% = 0.04–0.13) was detected, for the first time in Alpine ibex, in one subject. Protostrongylidae larval excretion varied significantly over time, with minimum L1 excretion in July. Individual median larval intensity ranged from 4.4 lpg to 82.2 lpg with Poulin's discrepancy index showing highly aggregated distribution patterns for Muellerius spp. (D = 0.283, CI95% = 0.760–0.895) and Protostrongylus spp. (D = 0.635, CI95% = 0.580–0.705). Presented data provide the necessary base point to further investigate how lungworm infection account for the different rates of progression of pneumonia in C. ibex. Individual aggregation of larval intensity must be further evaluated to determine whether these differences mirror different levels of parasitic infection related to individual differences in immune response, hormonal-states or genetic fitness.

Disentangling adaptation from drift in bottlenecked and reintroduced populations of Alpine ibex

Identifying local adaptation in bottlenecked species is essential for conservation management. Selection detection methods have an important role in species management plans, assessments of adaptive capacity, and looking for responses to climate change. Yet, the allele frequency changes exploited in selection detection methods are similar to those caused by the strong neutral genetic drift expected during a bottleneck. Consequently, it is often unclear what accuracy selection detection methods have across bottlenecked populations. In this study, simulations were used to explore if signals of selection could be confidently distinguished from genetic drift across 23 bottlenecked and reintroduced populations of Alpine ibex (Capra ibex). The meticulously recorded demographic history of the Alpine ibex was used to generate comprehensive simulated SNP data. The simulated SNPs were then used to benchmark the confidence we could place in outliers identified in empirical Alpine ibex SNP data. Within the simulated dataset, the false positive rates were high for all selection detection methods but fell substantially when two or more methods were combined. True positive rates were consistently low and became negligible with increased stringency. Despite finding many outlier loci in the empirical Alpine ibex SNPs, none could be distinguished from genetic drift-driven false positives. Unfortunately, the low true positive rate also prevents the exclusion of recent local adaptation within the Alpine ibex. The baselines and stringent approach outlined here should be applied to other bottlenecked species to ensure the risk of false positive, or negative, signals of selection are accounted for in conservation management plans.

Capture Sequencing to Explore and Map Rare Casein Variants in Goats

Genetic variations in the four casein genes CSN1S1, CSN2, CSN1S2, and CSN3 have obtained substantial attention since they affect the milk protein yield, milk composition, cheese processing properties, and digestibility as well as tolerance in human nutrition. Furthermore, milk protein variants are used for breed characterization, biodiversity, and phylogenetic studies. The current study aimed at the identification of casein protein variants in five domestic goat breeds from Sudan (Nubian, Desert, Nilotic, Taggar, and Saanen) and three wild goat species [Capra aegagrus aegagrus (Bezoar ibex), Capra nubiana (Nubian ibex), and Capra ibex (Alpine ibex)]. High-density capture sequencing of 33 goats identified in total 22 non-synonymous and 13 synonymous single nucleotide polymorphisms (SNPs), of which nine non-synonymous and seven synonymous SNPs are new. In the CSN1S1 gene, the new non-synonymous SNP ss7213522403 segregated in Alpine ibex. In the CSN2 gene, the new non-synonymous SNPs ss7213522526, ss7213522558, and ss7213522487 were found exclusively in Nubian and Alpine ibex. In the CSN1S2 gene, the new non-synonymous SNPs ss7213522477, ss7213522549, and ss7213522575 were found in Nubian ibex only. In the CSN3 gene, the non-synonymous SNPs ss7213522604 and ss7213522610 were found in Alpine ibex. The identified DNA sequence variants led to the detection of nine new casein protein variants. New variants were detected for alpha S1 casein in Saanen goats (CSN1S1∗C1), Bezoar ibex (CSN1S1∗J), and Alpine ibex (CSN1S1∗K), for beta and kappa caseins in Alpine ibex (CSN2∗F and CSN3∗X), and for alpha S2 casein in all domesticated and wild goats (CSN1S2∗H), in Nubian and Desert goats (CSN1S2∗I), or in Nubian ibex only (CSN1S2∗J and CSN1S2∗K). The results show that most novel SNPs and protein variants occur in the critically endangered Nubian ibex. This highlights the importance of the preservation of this endangered breed. Furthermore, we suggest validating and further characterizing the new casein protein variants.