Molecular systematics of the Hyaenidae: relationships of a relictual lineage resolved by a molecular supermatrix

The four extant species of hyenas (Hyaenidae; Carnivora) form a morphologically and ecologically heterogeneous group of feliform carnivorans that are remnants of a formerly diverse group of mammalian predators. They include the aardwolf (Proteles cristatus), a termite-feeding specialist, and three species with a craniodental morphology adapted to cracking the bones of prey and/or carcasses, the spotted hyena (Crocuta crocuta), brown hyena (Parahyaena brunnea), and striped hyena (Hyaena hyaena). Hyenas have been the subject of a number of systematic studies during the last two centuries, due in large part to the extensive fossil record of the group, with nearly 70 described fossil species. Morphological studies incorporating both fossil and living taxa have yielded different conclusions regarding the evolutionary relationships among living hyenas. We used a molecular supermatrix comprised of seven nuclear gene segments and the complete mitochondrial cytochrome b gene to evaluate phylogenetic relationships among the four extant hyaenid species. We also obtained sequence data from representative species of all the main families of the Feliformia (Felidae, Herpestidae, and Viverridae) to estimate the sister group of the Hyaenidae. Maximum parsimony and maximum likelihood analyses of the supermatrix recovered identical topologies. Furthermore, Bayesian phylogenetic analyses of the supermatrix, with among-site rate variation among data partitions parameterized in three different ways, also yielded the same topology. For each phylogeny reconstruction method, all but two nodes received 100% bootstrap or 1.00 posterior probability nodal support. Within the monophyletic Hyaenidae, Parahyaena and Hyaena were joined together, with Crocuta as the sister to this clade, and Proteles forming the most basal lineage. A clade containing two species of mongoose (core Herpestidae) plus Cryptoprocta ferox (currently classified in Viverridae) was resolved as the sister group of Hyaenidae. The pattern of relationships among the three bone-cracking hyaenids (Crocuta, Hyaena, and Parahyaena) is incongruent with recent cladistic assessments based on morphology and suggests the need to reevaluate some of the morphological characters that have been traditionally used to evaluate relationships among hyenas. Divergence time estimates based on a Bayesian relaxed molecular clock indicates that hyaenids diverged from their feliform sister group 29.2 MYA, in the Middle Oligocene. Molecular clock estimates also suggest that the origin of the aardwolf is much more recent (10.6 MYA) than that implied by a cladistic analysis of morphology ( approximately 20 MYA) and suggests that the aardwolf is possibly derived from a bone and meat eating lineage of hyaenids that were present in the Late Miocene. [Hyaenidae; phylogeny; cytochrome b; nuclear gene segments; Proteles; Crocuta; Hyaena; Parahyaena.].     

Coprolites as a source of information on the genome and diet of the cave hyena

We performed high-throughput sequencing of DNA from fossilized faeces to evaluate this material as a source of information on the genome and diet of Pleistocene carnivores. We analysed coprolites derived from the extinct cave hyena (Crocuta crocuta spelaea), and sequenced 90 million DNA fragments from two specimens. The DNA reads enabled a reconstruction of the cave hyena mitochondrial genome with up to a 158-fold coverage. This genome, and those sequenced from extant spotted (Crocuta crocuta) and striped (Hyaena hyaena) hyena specimens, allows for the establishment of a robust phylogeny that supports a close relationship between the cave and the spotted hyena. We also demonstrate that high-throughput sequencing yields data for cave hyena multi-copy and single-copy nuclear genes, and that about 50 per cent of the coprolite DNA can be ascribed to this species. Analysing the data for additional species to indicate the cave hyena diet, we retrieved abundant sequences for the red deer (Cervus elaphus), and characterized its mitochondrial genome with up to a 3.8-fold coverage. In conclusion, we have demonstrated the presence of abundant ancient DNA in the coprolites surveyed. Shotgun sequencing of this material yielded a wealth of DNA sequences for a Pleistocene carnivore and allowed unbiased identification of diet.     

南京汤山驼子洞鬣狗粪化石的孢粉分析

南京汤山驼子洞洞穴堆积中鬣狗粪化石含有相对丰富的孢粉,推测草食性哺乳动物食用带有孢粉的植物后,经鬣狗的猎杀、摄食、消化和排泄,孢粉较好地保存在鬣狗粪中,形成粪化石,成为洞穴地层的组成部分。虽然鬣狗粪化石中的孢粉含量不及湖沼相地层中丰富,但有几种植物的花粉保存较好且相对集中,如Pinus,Tsuga,Quercus,Carpinus,Artemisia,Cyperaceae,Polygonum,Polypodiaceae出现的频率较高。孢粉组合揭示早更新世南京地区植被主要是草原或森林-草地,气候凉干或半干旱半湿润,可以和地层中脊椎动物群反映的自然环境相互印证。在研究洞穴古环境的代用指标中,堆积物中的鬣狗粪化石中包含的孢粉是比较好的研究对象,对环境有一定的指示意义。     

The diet of the striped hyena in Nepal's lowland regions

Striped hyenas (Hyaena hyaena) are extremely rare in Nepal, and only a few people have studied them in their natural forest and grassland habitat. Their rarity is due to anthropogenic pressures such as hunting, habitat modification, being killed on roads, and depletion of their natural prey. Here, we studied the feeding ecology of hyenas in lowland, Nepal. We employed an opportunistic sampling to collect hyena scats in a range of habitats and the line transect sampling to identify the prey of the hyena in the study site. We collected 68 hyena scats between 2015 and 2018. Most of the hyena scat (39.7%) was found in the Churia Hill forest followed by riverbed (26.4%), mixed forest (14.7%), Sal (Shorea robusta)‐dominated forest (11.7%), and grassland area (7.3%). We found eleven mammalian prey species, plants, and some unidentified items in the hyena scats. The frequency of occurrence and relative biomass of the medium‐sized wild boar (Sus scrofa) were higher than other smaller prey species such as hare (Lepus nigricollis) and rhesus macaque (Macaca mulatta). Similarly, the proportion of large prey species such as nilgai (Boselaphus tragocamelus) in the hyena diet was lower compared with wild boar, hares, and rhesus macaques indicating medium‐sized wild boar is the most preferred prey species. Livestock contributed 17.3% of the total dietary biomass. Domesticated species such as goats, sheep, cows, and even dogs were found in the diet of hyenas. Predation of livestock by hyenas could cause conflict, especially if this ongoing issue continues in the future. Rather, more conservation effort is required in lowland areas of Nepal to protect the hyenas' natural prey species, particularly in wildlife habitats to reduce the lure of taking domestic livestock. Similarly, conservation education at the local level and active involvement of government authorities in the conservation of this species might be helpful to mitigate human–hyena conflict in the human‐dominated landscape.     

Non-invasive monitoring of glucocorticoid metabolites in brown hyaena (Hyaena brunnea) feces

The brown hyaena (Hyaena brunnea) is the least known of the large predators of southern Africa. The current IUCN status of the brown hyaena is “Near Threatened”, and there are conservation concerns related to a general lack of biological knowledge of the species. For instance, a better knowledge of the responses to environmental and social stressors would improve our abilities to sustainably manage brown hyaena populations in both captive and free‐ranging environments. We conducted adrenocorticotrophic hormone (ACTH) challenges in one female and one male adult brown hyaena at Lion Park Zoo, South Africa, to validate measurements of glucocorticoid metabolites (GCM) in brown hyaena feces via an enzyme immunoassay (EIA). We also measured gastrointestinal transit times (GIT times) and the GCM degradation in feces left in ambient temperature for up to 32 hr to more reliably assess the use of this assay as a tool for non‐invasive glucocorticoid measurements. Intramuscular injections of synthetic ACTH yielded GCM levels of 388% (female) and 2,682% (male) above baseline with peak increases occurring 25‐ to 40‐hr after injection. The time delay of fecal GCM excretion approximately corresponded with food transit time in the brown hyaenas. Fecal GCM levels declined significantly over time since defecation. Our results provided a good validation that fecal GCMs accurately reflect circulating glucocorticoid stress hormones in brown hyaenas, but we highlight that samples have to be frozen immediately after defecation to avoid bias in the measurements as a result of bacterial degredation. Zoo Biol 30:451–458, 2011. © 2010 Wiley‐Liss, Inc.     

The palaeoecology of the micromammals from the late middle Pleistocene site of Hoedjiespunt 1 (Cape Province, South Africa)

The palaeontological site of Hoedjiespunt 1 (HDP1) represents a fossilized hyaena lair. A rich mammalian fauna, including four hominid teeth, has been recovered from the site. Micromammals were recovered from the same sediments as the larger fauna. Taphonomic analysis suggests that the micromammal assemblages from HDP1 were accumulated by a barn owl. The barn owl produces micromammal assemblages that provide a broad sample of micromammals, within a certain size range, living in the hunting area of the owl. There are size-related and other biases inherent in the prey selection of this predator, and owls may roost in one area and hunt in another however, the barn owl has frequently been found to provide a better indication of micromammals living within an area than trapping. The micromammals from HDP1 were used to reconstruct the microhabitats in the vicinity of the site. Two taxonomic habitat indexes were used to assess the environment and dominant habitat types at Hoedjiespunt 1. The variability and adaptability of many of the southern African micromammals complicates interpretation of the results, however, it appears that the micromammals from the HDP1 fossil assemblages utilized habitats of open, scrub vegetation, and rocky and sandy areas. It is suggested that the environment was not markedly different from today, but it may have been relatively more arid. A comparison between HDP1 and other fossil sites in the area dating from the terminal Pleistocene to the Holocene indicates that HDP1 is lacking certain species that are common to all the other west coast fossil sites. There is some discrepancy in the environment indicated by the large mammals as compared that indicated by to the micromammals at the site. It is suggested that this discrepancy may reflect the fact that an owl is likely to have hunted in the vicinity of the hyaena den, probably in the more open areas around the roost site, whereas the macrofauna, accumulated by the further-ranging brown hyaena (Hyaena brunnea), represents environments from further afield.     

Patterns of relatedness and parentage in an asocial, polyandrous striped hyena population

We investigated patterns of relatedness and reproduction in a population of striped hyenas in which individuals are behaviourally solitary but form polyandrous spatial groups consisting of one adult female and multiple adult males. Group-mate males were often close relatives, but were unrelated or distantly related in some cases, indicating that male coalitions are not strictly a result of philopatry or dispersal with cohorts of relatives. Most male-female pairs within spatial groups were unrelated or only distantly related. Considering patterns of relatedness between groups, relatedness was significantly higher among adult males living in non-neighbouring ranges than among neighbouring males. Mean relatedness among male-female dyads was highest for group-mates, but relatedness among non-neighbouring males and females was also significantly higher than among dyads of opposite-sex neighbours. Female-female relatedness also increased significantly with increasing geographic separation. These unusual and unexpected patterns may reflect selection to settle in a nonadjacent manner to reduce inbreeding and/or competition among relatives for resources (both sexes), or mates (males). Finally, resident males fathered the majority of the resident female's cubs, but extra-group paternity was likely in 31% of the cases examined, and multiple paternity was likely in half of the sampled litters.     

Isotopic evidence for diet and subsistence pattern of the Saint-Césaire I Neanderthal: review and use of a multi-source mixing model

The carbon and nitrogen isotopic abundances of the collagen extracted from the Saint-Césaire I Neanderthal have been used to infer the dietary behaviour of this specimen. A review of previously published Neanderthal collagen isotopic signatures with the addition of 3 new collagen isotopic signatures from specimens from Les Pradelles allows us to compare the dietary habits of 5 Neanderthal specimens from OIS 3 and one specimen from OIS 5c. This comparison points to a trophic position as top predator in an open environment, with little variation through time and space. In addition, a comparison of the Saint-Césaire I Neanderthal with contemporaneous hyaenas has been performed using a multi-source mixing model, modified from Phillips and Gregg (2003, Oecologia 127, 171). It appears that the isotopic differences between the Neanderthal specimen and hyaenas can be accounted for by much lower amounts of reindeer and much higher amounts of woolly rhinoceros and woolly mammoth in the dietary input of the Neanderthal specimen than in that of hyaenas, with relatively similar contributions of bovinae, large deer and horse for both predators, a conclusion consistent with the zooarchaeological data. The high proportion of very large herbivores, such as woolly rhinoceros and woolly mammoth, in Neanderthal's diet compare to that of the scavenging hyaenas suggests that Neanderthals could not acquire these prey through scavenging. They probably had to hunt for proboscideans and rhinoceros. Such a prey selection could result from a long lasting dietary tradition in Europe.     

Transient genital abnormalities in striped hyenas (Hyaena hyaena)

The highly masculinized genitalia of female spotted hyenas Crocuta crocuta is unique among mammals: Crocuta have no external vagina so urination, penile intromission and parturition take place through the clitoris, which mimics a fully erectile male penis. Among hyenids, virilization of external female genitalia has previously been observed only in Crocuta, so functional explanations of masculinization have focused on aspects of social ecology unique to the species. Here we first show that the striped hyena Hyaena hyaena exhibits both unusual similarity in male and female androgen concentrations and transient genital anomalies characterized by a convergence in genital appearance among young males and females. We then evaluate hypotheses regarding the evolution of genital masculinization in the Hyaenidae and other taxa. Hyaena are behaviorally solitary, so discovery of unusual genital development patterns in this species does not support any current evolutionary models for masculinization in Crocuta, which all rely on the trait originating within a highly social species. Some hypotheses can be modified so that masculinization in Crocuta represents an extreme elaboration of a preexisting trait, shared as a homology with Hyaena.