Rhesus macaque

The Rhesus macaque (Macaca mulatta), also called the Rhesus monkey, is one of the best-known species of Old World monkeys. It is listed as Least Concern in the IUCN Red List of Threatened Species in view of its wide distribution, presumed large population, and its tolerance of a broad range of habitats. Native to South, Central and Southeast Asia, troops of Macaca mulatta inhabit a great variety of habitats from grasslands to arid and forested areas, but also close to human settlements.

Characteristics
The Rhesus macaque is brown or grey in color and has a pink face, which is bereft of fur. Its tail is of medium length and averages between 20.7 and 22.9 cm. Adult males measure approximately 53 cm on average and weigh about 7.7 kg. Females are smaller, averaging 47 cm in length and 5.3 kg in weight. Rhesus macaques have on average 50 vertebrae. Their intermembral index (ratio of arms to legs) is 89%. They have dorsal scapula and a wide rib cage.

The Rhesus macaque has 32 teeth with a dental formula of 2.1.2.3/2.1.2.3 and bilophodont molars. The upper molars have four cusps: paracone, metacone, protocone and hypocone. The lower molars also have four cusps: metaconid, protoconid, hypoconid and entoconid.

Distribution and habitat
Rhesus macaques are native to northern India, Bangladesh, Pakistan, Nepal, Burma, Thailand, Afghanistan, Vietnam, southern China, and some neighboring areas. The Rhesus monkey has the widest geographic ranges of any nonhuman primate, occupying a great diversity of altitudes throughout Central, South and Southeast Asia. Inhabiting arid, open areas, Rhesus macaques may be found in grasslands, woodlands and in mountainous regions up to 2500 m in elevation. They are regular swimmers. Babies as young as a few days old can swim, and adults are known to swim over a half mile between islands, but are often found drowned in small groups where their drinking waters lie. Rhesus macaques are noted for their tendency to move from rural to urban areas, coming to rely on handouts or refuse from humans. They have become a pest in some areas, perceived as a possible risk to public health and safety. In Peninsular India they have extended their distribution range ast few decades in south of River Godavari and Tapti at the cost of the endemic bonnet macaque.

Distribution of subspecies and populations
The name rhesus is reminiscent of the Greek mythological king Rhêsos. However, the French naturalist Jean-Baptiste Audebert who applied the name to the species, stated that it had no meaning.

According to Zimmermann’s first description of 1780, the Rhesus macaque is distributed in eastern Afghanistan, Bangladesh, Bhutan, as far east as the Brahmaputra Valley in peninsular India, Nepal and northern Pakistan. Today, this is known as the Indian Rhesus macaque Macaca mulatta mulatta, which includes the morphologically similar Macacus rhesus villosus described by True in 1894 from Kashmir and Macaca mulatta mcmahoni described by Pocock in 1932 from Kootai, Pakistan. Several Chinese subspecies of Rhesus macaques have been described between 1867 and 1917. The molecular differences identified among populations however are alone not consistent enough to conclusively define any subspecies.

The Chinese subspecies can be divided in:
 * Macaca mulatta mulatta – is found in western and central China, in the south of Yunnan and southwest of Guangxi;
 * Macaca mulatta lasiota (Gray, 1868) – the West Chinese Rhesus macaque is distributed in the west of Sichuan, northwest of Yunnan, southeast of Qinghai; possibly synonymous with Macaca mulatta sanctijohannis (Swinhoe, 1867), if not with Macaca mulatta mulatta.
 * Macaca mulatta tcheliensis (Milne-Edwards, 1870) – the North Chinese Rhesus macaque lives in the north of Henan, south of Shanxi and near Beijing. Some consider it as the most endangered subspecies. Others consider it possibly synonymous with M. m. sanctijohannis, if not with M. m. mulatta.
 * Macaca mulatta vestita (Milne-Edwards, 1892) – the Tibetan Rhesus macaque lives in the southeast of Tibet, northwest of Yunnan (Deqing), and perhaps including Yushu; possibly synonymous with M. m. sanctijohannis, if not with M. m. mulatta.
 * Macaca mulatta littoralis (Elliot, 1909) – the South Chinese Rhesus macaque lives in Fujian, Zhejiang, Anhui, Jiangxi, Hunan, Hubei, Guizhou, northwest of Guangdong, north of Guangxi, northeast of Yunnan, east of Sichuan and south of Shaanxi; possibly synonymous with M. m. sanctijohannis, if not with M. m. mulatta.
 * Macaca mulatta brevicaudus, also referred to as Pithecus brevicaudus (Elliot, 1913) – lives in the Hainan Island and Wanshan Islands in Guangdong, and the islands near Hong Kong; may be synonymous with M. m. mulatta.
 * Macaca mulatta siamica (Kloss, 1917) – the Indochinese Rhesus macaque is distributed in Myanmar, in the north of Thailand and Vietnam, in Laos and in the Chinese provinces of Anhui, northwest Guangxi, Guizhou, Hubei, Hunan, central and eastern Sichuan, western and south-central Yunnan; possibly synonymous with M. m. sanctijohannis, if not with M. m. mulatta.

Feral colonies in the United States
Around the spring of 1938, a colony of Rhesus macaques were released in the Silver River State Park in Florida by a tour boat operator known locally as "Colonel Tooey" to enhance his "Jungle Cruise". A traditional story that the monkeys were released for scenery enhancement in the Tarzan movies that were filmed at that location is false, as the only Tarzan movie filmed in the area, 1939's Tarzan Finds a Son! contains no Rhesus macaques. In addition, various colonies of Rhesus and other monkey species are speculated to be the result of zoos and wildlife parks destroyed in hurricanes, most notably Hurricane Andrew.

There is also a notable colony of Rhesus macaques on Morgan Island, one of the Sea Islands in the South Carolina Lowcountry. They were imported in the 1970s for use in local labs and are by all accounts thriving.

Ecology and behavior
Rhesus macaques are diurnal animals, and both arboreal and terrestrial. They are quadrupedal and, when on the ground, they walk digitigrade and plantigrade. They are mostly herbivorous feeding on mainly fruit, but also eating seeds, roots, buds, bark, and cereals. It has been estimated that they consume around 99 different plant species in 46 families. During the monsoon season, they get much of their water from ripe and succulent fruit. Macaque living far from water sources lick dewdrops from leaves and drink rain water accumulated in tree hollows. They have also been observed eating termites, grasshoppers, ants and beetles. When food is abundant, they are distributed in patches and forage throughout the day in their home range. They drink water when foraging and gather around streams and rivers. Rhesus macaques have specialized pouch-like cheeks, allowing them to temporarily hoard their food.

In psychological research, Rhesus macaques have demonstrated a variety of complex cognitive abilities, including the ability to make same-different judgments, understand simple rules, and monitor their own mental states. They have even been shown to demonstrate self-agency, an important type of self-awareness.

Group structure
Like other macaques, Rhesus troops comprise a mixture of 20–200 males and females. Females may outnumber the males by a ratio of 4:1. Males and females both have separate hierarchies. Females have highly stable matrilineal hierarchies in which a female’s rank is dependent on the rank of her mother. In addition, a single group may have multiple matrilineal lines that exist in a hierarchy, and a female outranks any unrelated females that rank lower than her mother. Rhesus macaques are unusual in that the youngest females tend to outrank their older sisters. This is likely because young females are more fit and fertile. Mothers seem to prevent the older daughters from forming coalitions against her. The youngest daughter is the most dependent on the mother, and would have nothing to gain from helping her siblings in overthrowing their mother. Since each daughter had a high rank in their early years, rebelling against their mother is discouraged. Juvenile male macaques also exist in matrilineal lines but once they reach 4–5 years of age they are driven out of their natal groups by the dominant male. Thus adult males gain dominance by age and experience.

In the group, macaques position themselves based on rank. The Central Male Sub-group contains the 2-3 oldest and most dominant males who are co-dominant, along with females, their infants and juveniles. This sub-group occupies the center of the group and determines the movements, foraging and other routines. The females of this sub-group are also the most dominant of the entire group. The farther to the periphery a sub-group is, the less dominant it is. Sub-groups on the periphery of the central group are run by one dominant male who ranks lower than the central males, and who maintain order in the group and communicate messages between the central and peripheral males. A sub-group of subordinate, often sub-adult males occupy the very edge of the groups and have the responsibility of communicating with other macaque groups and make alarm calls.

Communication
Rhesus macaques interact using a variety of facial expressive, vocalizations and body postures, and gestures. Perhaps the most common facial expression the macaque makes is the "silent bared teeth" face. This is made between individuals of different social rank with the lower rank one giving the expression to its superior. A less dominant individual will also make a "fear grimace" accompanied by a scream to appease or redirect aggression. Another submissive behavior is the "present rump" where an individual raises its tail and exposes its genitals to the dominant one. A dominant individual will threaten another individual standing quadrupedally making a silent "open mouth stare" accompanied by the tail sticking straight. During movements, macaques will make "coos" and "grunts". These are also made during affiliative interactions and approaches before grooming. When they find rare food of high-quality, macaque will emit "Warbles," "harmonic arches," or "chirps." When in threatening situations, macaques will emit a single loud, high-pitched sounds called a "shrill bark". "Screeches," "screams," "squeaks," "pant-threats," "growls," and "barks" are when during aggressive interactions. Infants make "geckers" during weaning conflicts.

Reproduction
Adult male macaques try to maximize their reproductive success by entering into consort pairs with females, both in and outside the breeding period. Females prefer to mate with males that will increase the survival of their young. Thus a consort male provides resources for his female and protects her from predators. Larger, more dominant males are more likely to provide for the females. The breeding period can last up to 11 days, and a female usually mates with four males during that time. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. Female macaques first breed when they are four years old, and reach menopause at around 25 years of age. Male macaques generally play no role in raising the young but do have peaceful relationships with the offspring of their consort pairs.

Mothers with one or more immature daughters in addition to their infants are in contact with their infants less than those with no older immature daughters. This is because the mothers may pass the parenting responsibilities to her daughters. High-ranking mothers with older immature daughters also reject their infants significantly more than those without older daughters, and tend to begin mating earlier in the mating season than expected based on their dates of parturition the preceding birth season. Infants farther from the center of the groups are more vulnerable to infanticide from outside groups. Some mothers abuse their infants which is believed to be the result of controlling parenting styles.

In science
The Rhesus macaque is well known to science. Due to its relatively easy upkeep in captivity, its wide availability and its closeness to humans anatomically and physiologically, it has been used extensively in medical and biological research on human and animal health-related topics. It has given its name to the Rhesus factor, one of the elements of a person's blood group, by the discoverers of the factor, Karl Landsteiner and Alexander Wiener. The Rhesus macaque was also used in the well-known experiments on maternal deprivation carried out in the 1950s by controversial comparative psychologist Harry Harlow. Other medical breakthroughs make possible by the use of the Rhesus macaque include:
 * development of the rabies, smallpox, and polio vaccines
 * creation of drugs to manage HIV/AIDS
 * understanding of the female reproductive cycle and development of the embryo and the propagation of embryonic stem cells.

The U.S. Army, the U.S. Air Force, and NASA launched Rhesus macaques into outer space during the 1950s and 60s, and the Soviet/Russian space program launched them into space as recently as 1997 on the Bion missions. One of these primates ("Able") who was launched on a suborbital spaceflight in 1959 was one of the two first living beings (along with "Miss Baker" on the same mission) to travel in space and return alive.

In January 2000, the Rhesus macaque became the first cloned primate with the birth of Tetra. January 2001 saw the birth of ANDi, the first transgenic primate; ANDi carries foreign genes originally from a jellyfish.

Though most studies of the Rhesus macaque are from various locations in northern India, some knowledge of the natural behavior of the species comes from studies carried out on a colony established by the Caribbean Primate Research Center of the University of Puerto Rico on the island of Cayo Santiago, off Puerto Rico. There are no predators on the island, and humans are not permitted to land except as part of the research programmes. The colony is provisioned to some extent, but about 50% of its food comes from natural foraging. In other more controlled settings, these macaques often enjoy Fig Newtons, and are particularly keen on "pouching" large quantities of marshmallow.

Sequencing the genome
Work on the genome of the Rhesus macaque was completed in 2007, making Rhesus macaque the second non-human primate to have its genome sequenced. Humans and macaques apparently share about 93% of their DNA sequence and shared a common ancestor roughly 25 million years ago.

Comparison of Rhesus macaques, chimpanzees and humans revealed the structure of ancestral primate genomes, positive selection pressure and lineage-specific expansions and contractions of gene families.

"The goal is to reconstruct the history of every gene in the human genome," said Evan Eichler, University of Washington, Seattle. DNA from different branches of the primate tree will allow us "to trace back the evolutionary changes that occurred at various time points, leading from the common ancestors of the primate clade to Homo sapiens," said Bruce Lahn, University of Chicago.

After the human and chimpanzee genomes were sequenced and compared, it was usually impossible to tell whether differences were the result of the human or chimpanzee gene changing from the common ancestor. After the Rhesus macaque genome was sequenced, 3 genes could be compared. If 2 genes were the same, they are presumed to be the original gene.

The chimpanzee and human genome diverged 6 million years ago. They have 98% identity and many conserved regulatory regions. Comparing the macaque and human genome, which diverged 25 million years ago and had 93% identity, further identified evolutionary pressure and gene function.

Like the chimpanzee, changes were on the level of gene rearrangements rather than single mutations. There were frequent insertions, deletions, changes in the order and number of genes, and segmental duplications near gaps, centromeres and telomeres. So macaque, chimpanzee and human chromosomes are mosaics of each other.

Surprisingly, some normal gene sequences in healthy macaques and chimpanzees cause profound disease in humans. For example, the normal sequence of phenylalanine hydroxylase in macaques and chimpanzees is the mutated sequence responsible for phenylketonuria in humans. So humans must have been under evolutionary pressure to adopt a different mechanism.

Some gene families are conserved or under evolutionary pressure and expansion in all 3 primate species, while some are under expansion uniquely in human, chimpanzee or macaque.

For example, cholesterol pathways are conserved in all 3 species (and other primate species). In all 3 species, immune response genes are under positive selection, and genes of T cell-mediated immunity, signal transduction, cell adhesion, and membrane proteins generally. Genes for keratin, which produce hair shafts, were rapidly evolving in all 3 species, possibly because of climate change or mate selection. The X chromosome has 3 times more rearrangements than other chromosomes. The macaque gained 1,358 genes by duplication.

Triangulation of human, chimpanzee and macaque sequences showed expansion of gene families in each species.

The PKFP gene, important in sugar (fructose) metabolism, is expanded in macaques, possibly because of their high-fruit diet. So are genes for the olfactory receptor, cytochrome P450 (which degrades toxins), and CCL3L1-CCL4 (associated in humans with HIV susceptibility).

Immune genes are expanded in macaques, relative to all 4 great ape species. The macaque genome has 33 major histocompatibility genes, 3 times that of human. This has clinical significance because the macaque is used as an experimental model of the human immune system.

In humans, the PRAME (preferentially expressed antigen of melanoma) gene family is expanded. It is actively expressed in cancers but normally testis-specific, possibly involved in spermatogenesis. The PRAME family has 26 members on human chromosome 1. In the macaque, it has 8, and has been very simple and stable for millions of years. The PRAME family arose in translocations in the common mouse-primate ancestor 85 million years ago, and is expanded on mouse chromosome 4.

Agilent and Affymetrix have macaque DNA microarrays with 20,000 gene sequences, and they are used in macaque research. For example, Michael Katze of University of Washington, Seattle, infected macaques with 1918 and modern influenza. The DNA microarray showed the macaque genomic response to human influenza on a cellular level in each tissue. Both viruses stimulated innate immune system inflammation, but the 1918 flu stimulated stronger and more persistent inflammation, causing extensive tissue damage, and it did not stimulate the interferon-1 pathway. The DNA response showed a transition from innate to adaptive immune response over 7 days.