Phylogeography and demographic history of macaques, fascicularis species group, in East Asia: Inferred from multiple genomic markers.

Climate changes at larger scales have influenced dispersal and range shifts of many taxa in East Asia. The fascicularis species group of macaques is composed of four species and is widely distributed in Southeast and East Asia. However, its phylogeography and demographic histories are currently poorly understood. Herein, we assembled autosomal, mitogenome, and Y-chromosome data for 106 individuals, and combined them with 174 mtDNA dloop haplotypes of this species group, with particular focus on the demographic histories and dispersal routes of Macaca fuscata, M. cyclopis, and M. mulatta. The results showed: (1) three monophyletic clades for M. fuscata, M. cyclopis, and M. mulatta based on the multiple genomics analyses; (2) the disparate demographic trajectories of the three species after their split ∼1.0 Ma revealed that M. cyclopis and M. fuscata were derived from an ancestral M. mulatta population; (3) the speciation time of M. cyclopis was later than that of M. fuscata, and their divergence time occurred at the beginning of "Ryukyu Coral Sea Stage" (1.0-0.2 Ma) when the East China Sea land bridge was completely submerged by the sea level rose; and (4) the three parallel rivers (Nujiang, Lancangjiang, and Jinshajiang) of Southwestern China divided M. mulatta into Indian and Chinese genetic populations ∼200 kya. These results shed light on understanding not only the evolutionary history of the fascicularis species group but also the formation mechanism of faunal diversity in East Asia during the Pleistocene.

Spondyloarthritis in Taihangshan Macaques (Macaca mulatta tcheliensis).

The rhesus macaque (Macaca mulatta) is the most widely distributed nonhuman primate species, and captive populations play an important role in biomedical research due to close phylogenetic and physiological similarity to human beings. However, to our best knowledge, the spondyloarthritis (SpA) in rhesus macaques has been exclusively reported in captive or semicaptive populations rather than wild counterparts. In the present study, we report 2 cases of SpA observed in Taihangshan macaques (Macaca mulatta tcheliensis) inhabiting the Taihangshan Macaque National Nature Reserve, Henan Province, China. Among these 2 cases, one can be diagnosed as ankylosing spondylitis (AS) following accepted medical criteria, and another case showed evident fusion at the pubic symphysis which could be specific to rhesus macaque AS. We discuss the potential causes leading directly or indirectly to the development of SpA.

Neonatal nipple preference and maternal cradling laterality in wild Taihangshan macaques (Macaca mulatta tcheliensis).

Lateralized behavior is considered an observable phenotype of cerebral functional asymmetry and has been documented in many mammalian species. In the present study, we examined evidence of lateralization in neonatal nipple contact, maternal cradling, and the relationship between these two behaviors during the first 12 weeks of life in wild Taihangshan macaques (Macaca mulatta tcheliensis). The results showed that across our sample of nine mother-infant dyads: (1) Seven of nine neonates exhibited a significant left-side nipple preference during the first 12 weeks of life, whereas eight of nine mothers displayed a significant right-side cradling preference; (2) at the population level, there was a significant preference for left nipple contact by neonatal Taihangshan macaques and a significant right-hand maternal cradling preference; (3) at the population level, there was a nonsignificant negative correlation between neonatal nipple preference and maternal cradling bias; and (4) the strength of individual neonatal nipple preference and maternal cradling laterality were not correlated. We conclude that asymmetry in nipple contact of Taihangshan macaques occurs early in behavioral development. Given that infant Taihangshan macaques are able to nurse and cling unassisted to their mothers within a few days after birth, it appears that the infant rather than its mother is responsible for determining a nipple-side preference. Our results indicating a left-side nipple bias in 78% of wild neonatal Taihangshan macaques are most consistent with the heartbeat hypothesis.

Dietary specialization drives multiple independent losses and gains in the bitter taste gene repertoire of Laurasiatherian Mammals.

BACKGROUND: Bitter taste perception is essential for species with selective food intake, enabling them to avoid unpalatable or toxic items. Previous studies noted a marked variation in the number of TAS2R genes among various vertebrate species, but the underlying causes are not well understood. Laurasiatherian mammals have highly diversified dietary niche, showing repeated evolution of specialized feeding preferences in multiple lineages and offering a unique chance to investigate how various feeding niches are associated with copy number variation for bitter taste receptor genes. RESULTS: Here we investigated the evolutionary trajectories of TAS2Rs and their implications on bitter taste perception in whole-genome assemblies of 41 Laurasiatherian species. The number of intact TAS2Rs copies varied considerably, ranging from 0 to 52. As an extreme example of a narrow dietary niche, the Chinese pangolin possessed the lowest number of intact TAS2Rs (n = 2) among studied terrestrial vertebrates. Marine mammals (cetacea and pinnipedia), which swallow prey whole, presented a reduced copy number of TAS2Rs (n = 0-5). In contrast, independent insectivorous lineages, such as the shrew and insectivorous bats possessed a higher TAS2R diversity (n = 52 and n = 20-32, respectively), exceeding that in herbivores (n = 9-22) and omnivores (n = 18-22). CONCLUSIONS: Besides herbivores, insectivores in Laurasiatheria tend to have more functional TAS2Rs in comparison to carnivores and omnivores. Furthermore, animals swallowing food whole (cetacean, pinnipedia and pangolin) have lost most functional TAS2Rs. These findings provide the most comprehensive view of the bitter taste gene repertoire in Laurasiatherian mammals to date, casting new light on the relationship between losses and gains of TAS2Rs and dietary specialization in mammals.

Evidence of Placentophagia and Mother-Infant Cannibalism in Free-Ranging Macaca mulatta tcheliensis in Mount Taihangshan, Jiyuan, China.

Placentophagia or the consumption of the afterbirth is reported in many primate species, whereas cannibalism is a relatively rare event. Based on our field observations over the course of 3 years, we present evidence of placentophagia and mother-infant cannibalism in a free-ranging population of the Taihangshan macaque, Macaca mulatta tcheliensis, in the Mt. Taihangshan area, Jiyuan, Henan, China. We documented 1 case in which a mother consumed the afterbirth of her infant. In a second instance, we observed a fresh placenta discarded on the ground by an unknown individual. We also present a description of the first documented instance of mother-infant cannibalism in the same group of free-ranging rhesus macaques.

Colonization history shaped the immunity of the western house mouse.

The general development of immune response in the short and long term is a product of the antigenic environment in which a species resides. Colonization of a novel antigenic environment by a species would be expected to alter the immune system. Animals that successfully adapt their immune responses will successfully colonize new locations. However, founder events associated with colonization by limited numbers of individuals from a source population will constrain adaptability. How these contradicting forces shape immunity in widely distributed species is unknown. The western house mouse (Mus musculus domesticus) spread globally from the Indo-Pakistani cradle, often in association with human migration and settlement. In the present study, we tested the hypothesis that wild-derived outbred laboratory populations of house mice from their original range (Iran) and historically recent European invasive populations (from France and Germany) present differences in immune functional diversity corresponding to recent historical founder events in Europe and movement to novel antigenic environments. We found that (1) European mice had lower total white blood cell (WBC) counts but higher immunoglobulin E concentrations than their Iranian counterparts, and (2) there were no significant differences in the measured immunological parameters among European populations. The results indicate that founder events in European mice and selection pressure exerted by the composition of local parasitic helminth communities underlie the observed patterns.

The phylogenetic relationship and demographic history of rhesus macaques (Macaca mulatta) in subtropical and temperate regions, China.

Pleistocene climatic oscillations exerted significant influences on the genetic structure and demography of rhesus macaque (Macaca mulatta) in eastern China. However, the evolutionary history of rhesus macaques in subtropical and temperate China remained unclear and/or controversial. Herein, we analyzed the autosomes, mitochondrial genomes, and Y-chromosomes from 84 individuals of Chinese rhesus macaque. The results revealed that (1) all individuals were clustered into pan-west and pan-east genetic groups, which exhibited Shaanxi Province as the northernmost region of western dispersal route of rhesus macaques in China; (2) in subtropical and temperate China, rhesus macaques were divided into four lineages (TH, DB, HS, and QL), and their divergence times corresponded to the Penultimate Glaciation (300-130 kya) and Last Glaciation (70-10 kya), respectively; (3) the individuals from Mt. Taihangshan (TH) are closely related to individuals from Mt. Dabashan (DB) in the autosomal tree, rather than individuals from Mt. Huangshan (HS) as indicated by the mitogenome tree, which supports the hypothesis that the ancestral rhesus macaques radiated into Mt. Taihangshan from Mt. Huangshan via Mt. Dabashan; and (4) the demographic scenario of the four lineages showed the ancestral rhesus macaques bottleneck and expansion corresponding to the suitable habitat reduction and expansion, which confirmed they had experienced northward recolonization and southward retreat events from Mt. Huangshan area via Northern China Plain to Northernmost China along with Pleistocene glacial cycles. This study provides a new insight into understanding how Pleistocene glaciation has influenced faunal diversity in subtropical and temperate China, especially for those exhibiting differential patterns of sex dispersal.

DNA metabarcoding reveals the seasonal variation of dietary composition of Taihangshan macaque (Macaca mulatta tcheliensis), Jiyuan, north China.

Dietary analysis in wildlife is fundamental for understanding their flexible response to seasonal changes and developing effective conservation management measures. Taihangshan macaque (Macaca mulatta tcheliensis) is the northernmost population of rhesus macaque, currently only distributed in the southern Mt. Taihangshan area. This area belongs to a semi-arid region resulting in limited plant food availability for Taihangshan macaques, with seasonal variation. Herein, we used a chloroplast trnL DNA metabarcoding approach to identify the plant diet diversity and composition from 100 fecal samples of Taihangshan macaque in four seasons (spring, summer, autumn, and winter) from 2020 to 2021. The results revealed that (1) a total of 48 distinct families, 88 genera, and 52 species within the 105 food items that were consumed by Taihangshan macaques throughout the year; (2) the diversity of food items exhibited significant differences across the four seasons; (3) Rosaceae, Rhamnaceae, Fagaceae, and Poaceae are the preferential food items for Taihangshan macaques and have different relative abundances, fluctuating with seasonal variation. DNA metabarcoding can expand our understanding of the repertoire of food items consumed by Taihangshan macaques by detecting some consumed food items in this population that were not yet discovered using traditional methods. Therefore, the integrative results from traditional methods and DNA metabarcoding can provide a fundamental understanding of dietary composition to guide the conservation management of Taihangshan macaques.

Reproductive parameters of female Macaca mulatta tcheliensis in the temperate forest of Mount Taihangshan, Jiyuan, China.

The remaining population of Macaca mulatta tcheliensis, approximately 3,000 individuals, is currently confined to the southern region of Mount Taihangshan, northern China. Using data collected from February 2003 to November 2012, we examined female reproductive characteristics in a seasonally food supplemented free-ranging group of M. m. tcheliensis (Wangwu 1, WW-1), inhabiting the Taishangshan Macaque National Nature Reserve (TMNNR), Jiyuan, China. We tested a series of predictions regarding the degree to which M. m. tcheliensis is best considered as a "strict income breeder," a "relaxed income breeder" or a "capital breeder." This group was comprised 18 adult females who produced 64 infants over the 10-year study period. In our study group (WW-1) adult female macaques gave birth to an average of 0.71 ± 0.26 infants per year. Infant mortality was 13.4 ± 19.3%. The age at first birth for mothers was 4.9 ± 0.5 years old. The mean inter-birth interval (IBI) was 15.4 ± 4.9 months. Based on the fact M. m. tcheliensis is a strictly seasonal breeder (76.6% of births occurred between April and May) with infants born during a time of the year when food availability appears to be high, and that their IBI is intermediate in length compared with other macaque populations, our results suggest that M. m. tcheliensis follows a birth pattern most consistent with a "relaxed income breeder" strategy.

Genetic structure and recent population demographic history of Taihangshan macaque (Macaca mulatta tcheliensis), North China.

Massive actions have been and are being taken into protecting the world's primates from extinction, while the study of the properties of genetic diversity, demographic history, and ecological relationships will benefit the understanding of the long-term survival of a species. The Taihangshan macaque (Macaca mulatta tcheliensis), a subspecies of rhesus macaque (Macaca mulatta), is endemic to China and currently restricted to southern Mt. Taihangshan area. Herein, we evaluated the genetic diversity, population structure, and demographic history of this subspecies using mitochondrial (Cytb and high variable region I: HVR I) and nuclear markers (microsatellite loci) of 131 individuals collected from 9 localities covering the distribution range of this subspecies. Both phylogenetic analyses and genetic assignment revealed that the wild populations of Taihangshan macaques could be divided into 2 major highly divergent clades, THS-east and THS-west. Low genetic diversity (π: 0.00266 ± 0.00016) but high haplotype diversity (Hd : 0.80352 ± 0.015) were detected in the Taihangshan macaques, particularly in THS-east. Analyses of demographic history suggested that the Taihangshan macaques experienced first a stable historical population size from Holocene to early 19th century but a subtle decline and then slight growth in the recent 200 years. We suggest that bridging the neighbor populations (i.e. setting corridors) would facilitate the male-mediated gene flow and subsequently increase the genetic diversity of the Taihangshan macaque populations.

Effects of social and climatic factors on birth sex ratio in Macaca mulatta in Mount Taihangshan area.

Sex allocation theory predicts the optimal investment to male and female offspring. However, a biased sex ratio requires explanations as to why the deviation occurs. Rhesus macaque (Macaca mulatta) is the most widely distributed nonhuman primate species and the Taihangshan macaque (Macaca mulatta tcheliensis) occupies the northern limit of all rhesus macaque natural populations worldwide. We observed one macaque troop (Wangwu-1 [WW-1]) inhabiting Taihangshan Macaque National Nature Reserve and recorded all birth events and the sex of newborn macaques from 2004 to 2013. Our aim was to apply the Trivers-Willard hypothesis to this free-ranging rhesus macaque troop, and to understand the relationship between climatic parameters (precipitation and temperature) and birth sex ratio. We found that the total newborn macaques showed a female-biased sex ratio at birth in the WW-1 troop, but there were no significant biased birth sex ratios in all matriarchs and in high-ranking and middle-ranking matrilineal units. However, the low-ranking macaque matrilineal unit was significantly female-biased. Moreover, we found that the annual precipitation of the previous year was positively associated with the birth sex ratio, and there was an interactive effect of troop size and current winter temperature on the birth sex ratio. The underlying mechanisms for the effects of social and climatic factors on birth sex ratio could be complex, and we discuss several plausible explanations.

Establishment of a microsatellite set for noninvasive paternity testing in free-ranging Macaca mulatta tcheliensis in Mount Taihangshan area, Jiyuan, China.

BACKGROUND: Within multi-male and multi-female mammalian societies, paternity assignment is crucial for evaluating male reproductive success, dominance hierarchy, and inbreeding avoidance. It is, however, difficult to determine paternity because of female promiscuity during reproduction. Noninvasive molecular techniques (e.g., fecal DNA) make it possible to match the genetic father to his offspring. In the current study, a troop of free-ranging Taihangshan macaques (Macaca mulatta tcheliensis) in Mt. Taihangshan area, Jiyuan, China, was selected for studying the paternity. We successfully screened a set of microsatellite loci from fecal DNA and evaluated the efficiency of these loci for paternity testing using clearly recorded data of maternity. RESULTS: The results showed that: 1) ten loci out of 18 candidate microsatellite loci were amplified successfully in the fecal samples of Taihangshan macaques. The error probability in maternity assignments and paternity testing was very low as indicated by their power of discrimination (0.70 to 0.95), power of exclusion (0.43 to 0.84), and the values of polymorphic information content ranging from 0.52 to 0.82; 2) the combined probability of exclusion in paternity testing for ten qualified loci was as high as 99.999%, and the combined probability of exclusion reached 99.99% when the seven most polymorphic loci were adopted; 3) the offspring were assigned to their biological mother correctly and also matched with their genetic father. CONCLUSIONS: We concluded that the ten polymorphic microsatellite loci, especially a core set of seven most polymorphic loci, provided an effective and reliable tool for noninvasive paternity testing in free-ranging rhesus macaques.