Black Snub Nosed Monkeys

As you may know, primates have a large head to body ratio — larger than other mammals. This makes birthing a challenge as larger head has to pass through the birth canal. As a result, labor is far more laborious and risky and primate infants are born less developed than other mammals.

Assistance during labor has been seen a few time before.  In one case, a male cottontop tamarin pulled his infant’s shoulders. Another report documents the grooming of a female capped langur during birth, perhaps in trying to ease the distress. While primates offer some help during birth, it has been seen in that male Djungarian hamsters regularly assist with deliveries, pulling infants out with their front paws and incisors.

In the paper, Xiao and colleague document the 15 minute birthing of a first time mother. She climbs up a rhododendron tree, faintly calling. Her calls turn into screams within 10 minutes. An experienced female black snub-nosed monkey climbs up to this screaming mother. As the new mother began crowning, the experienced female sat beside.

The head, once fully exposed, was grabbed by the midwife, who pulled the baby out with both hands. She progressed to rip open the birth membranes. The new mother reclaimed the infant within a minute, and severed the umbilical cord. She ate the placenta as the midwife descended.

Black snub-nosed monkeys live in bands. These bands are as large as 300-400, but are often sub-divided into smaller groups of 10 individuals. These groups are often harems. The female black snub-nosed monkeys tend to stay in the group they were born in. It is likely, therefore, that females in a group are closely related and to have strong social bonds and act upon calledkin selection. Furthermore, it has been observed that juvenile females closely watching births. During this particular birth, two other females watched it happen.

Ding, W., Yang, L., & Xiao, W. (2013). Daytime birth and parturition assistant behavior in wild black-and-white snub-nosed monkeys (Rhinopithecus bieti) Yunnan,China Behavioural Processes DOI: 10.1016/j.beproc.2013.01.006

Two Bonobos {Pan paniscus} vocalizing. Lola Ya Bonobo Sanctuary, Kinshasa, DR of Congo, 2007

The bonobo genome is sequenced. The letter reporting was recently published in Nature, and is available openly under the title, “The bonobo genome compared with the chimpanzee and human genomes.”  Kay Prüfer from the Max Plank Institute for Evolutionary Anthropologyis the lead author. There are some interesting preliminary comparisons such as:

• Bonobos and chimps have 99.6% sequence similarity
• Bonobos and humans have 98.7% sequence similarity
• The split of bonobo and chimpanzee is confirmed to have approx. 1 million years ago, with no inbreeding occurring
• 6% of the bonobo genome has evidence of incomplete lineage sorting(when an allele does not match the population history of a species)
  • This has lead to the observation that  ~1.6% of the bonobo genome is more similar to humans than chimpanzees

a, Schematic description of ILS states and percentage of bases assigned to each state. b, Effective population sizes and split times inferred from ILS and based on a molecular clock with a mutation rate of 10−9 yr−1. Myr, million years. We note that other estimates of mutation rates will correspondingly affect the estimates of the split times. c, Overlap between predicted ILS transposons and the closest HMM ILS assignments within 100 bp of a transposon insertion. d, Proportion of ILS in exons, introns and across the whole genome, counted within ~1-Mb segments of alignment (Supplementary Information, section 8). e, Proportion of ILS dependent on recombination rates. Errors, 95% confidence interval.

Prüfer, K., Munch, K., Hellmann, I., Akagi, K., Miller, J., Walenz, B., Koren, S., Sutton, G., Kodira, C., Winer, R., Knight, J., Mullikin, J., Meader, S., Ponting, C., Lunter, G., Higashino, S., Hobolth, A., Dutheil, J., Karakoç, E., Alkan, C., Sajjadian, S., Catacchio, C., Ventura, M., Marques-Bonet, T., Eichler, E., André, C., Atencia, R., Mugisha, L., Junhold, J., Patterson, N., Siebauer, M., Good, J., Fischer, A., Ptak, S., Lachmann, M., Symer, D., Mailund, T., Schierup, M., Andrés, A., Kelso, J., & Pääbo, S. (2012). The bonobo genome compared with the chimpanzee and human genomes Nature DOI: 10.1038/nature11128

Credit: © Mission Paléontologique Franco-Myanmar (MPFM) The Pondaung sediment at Thamingyauk locality, Myanmar.

The species has been named Afrasia djijidae based upon 4 teeth recovered from the site. Afrasia pays homage to the ancestry of these early anthropoids who are now found intercontinentally, between Africa and Asia. And djijidae refers to memory of a young girl from village of Mogaung in central Myanmar. In comparing the teeth to other primates an remarkable discovery was made…

Afrasia‘s teeth closely resemble those of the 38-million-year-old Afrotarsius libycus. The shape of the Asian Afrasia and the North African Afrotarsius fossils shows both species survived off insects and weighed around 100 grams or so, about size of a modern tarsier. A. libycus was recently discovered in the Sahara, where it was more ecologically diverse and suggesting that they actually originated elsewhere. The close similarity in dentition between Afrasia and Afrotarsius raises the possibility that early anthropoids colonized Africa from Asia.

Credit: © Mission Paléontologique Franco-Myanmar (MPFM) The close similarity between Afrasia (right) and Afrotarsius (left) now suggests that early anthropoids colonized Africa from Asia.

Credit: Mark A. Klinger, Carnegie Museum of Natural History  Shown here, Afrotarsius (top left), Karanesia (top right), Biretia (bottom left), and Talahpithecus (bottom right) reconstructions shown feeding along the shoreline forest.

A open question that remains is just how was Africa colonized from Asia? Around 38-37 million years ago the Tethys Sea separated the two continents. The authors write how the primates could have island hopped by swimming and using logs as rafts. I think this is an outlandish idea. But they supplement this hypothesis by stating how such as Asian rodents and extinct piglike animals known as anthracotheres colonized Africa.

Another open question is how come the Afrasia species and other ancestral primates did not lead way to their lineage of primates, much like the African counter parts? The authors address this question by stating that a glacial event 34 million years ago, dramatically cooled the climate. This drop in temperature affected Asia more than Africa, leading to the disappearance of Asian anthropods. And for anthropoids like gibbons and orangutans in Asia now, such as gibbons and orangutans immigrated from Africa some 20 million years ago.

Chaimanee, Y., Chavasseau, O., Beard, K., Kyaw, A., Soe, A., Sein, C., Lazzari, V., Marivaux, L., Marandat, B., Swe, M., Rugbumrung, M., Lwin, T., Valentin, X., -Maung-Thein, Z., & Jaeger, J. (2012). Late Middle Eocene primate from Myanmar and the initial anthropoid colonization of Africa Proceedings of the National Academy of Sciences DOI: 10.1073/pnas.1200644109

Baby gorilla sleeping on his mother, by bartdubelaar

During a 4 month observation of these gorillas, it was observed that elder gorillas used different gestures to start and stop play. To engage in play, the older gorillas would typically slapp others while making a “play face” or somersault. And to end play, these gorillas would place hand on the other gorilla’s head. But when engaged with infants, each older gorilla used repeated touch-based gestures more. As explained in the abstract,

“Infant-directed speech is a linguistic phenomenon in which adults adapt their language when addressing infants in order to provide them with more salient linguistic information and aid them in language acquisition. Adult-directed language differs from infant-directed language in various aspects, including speech acoustics, syntax, and semantics. The existence of a “gestural motherese” in interaction with infants, demonstrates that not only spoken language but also nonvocal modes of communication can become adapted when infants are recipients. Rhesus macaques are so far the only nonhuman primates where a similar phenomenon to “motherese” has been discovered: the acoustic spectrum of a particular vocalization of adult females may be altered when the addressees are infants. The present paper describes how gorillas adjust their communicative strategies when directing intentional, nonvocal play signals at infants in the sense of a “nonvocal motherese.” Animals of ages above infancy use a higher rate of repetitions and sequences of the tactile sensory modality when negotiating play with infants. This indicates that gorillas employ a strategy of infant-specific communication.”

A video of this behavior is provided by the New Scientist.

I used to work with two gorillas who both extensively used gestures to relay communication. So, I assume all who have taken care of these great apes would appreciate that it is is vital for all gorilla infants to identify different signals, similar to how human infants gain expertise spoken (an non-spoken) language. In both great apes, simplifying these forms of communication into baby talk, and repeating possibly help in solidifying associations.

LUEF, E., & LIEBAL, K. (2012). Infant-Directed Communication in Lowland Gorillas (Gorilla gorilla): Do Older Animals Scaffold Communicative Competence in Infants? American Journal of Primatology DOI: 10.1002/ajp.22039

As described in a recently published paper in Biology Letters, the Philippine Tarsier (Tarsius syrichta) has been found to communicate through extremely high pitched vocalisations in the ultrasound domain, undetectable by human ear. These presumed mute primates baffled primatologists… How can such lack of calls be observed when closely related species are clearly dependent on frequent vocal signals within the group? However the mystery was solved when upon further inspection, these little guys could be heard communicating among the highest frequency levels detected from any terrestrial mammals. It is now thought the extremes of these calls could allow conspecifics to communicate whilst remaining undetected by predators or prey and/or allow individuals to be more easily heard through background noise.

(Ramsier et al. 2012) Primate communication in the pure ultrasound.
DOI: 10.1098/rsbl.2011.1149

Pairs of chimpanzees (Pan troglodytes) where placed into testing rooms, separated by a mesh barrier. One individual had access to 30 tokens, divided into two separate colours – all of which could be given to the experimenter in exchange for food. Half of these when exchanged resulted in a selfish outcome in which only the individual handing the token received a reward, whereas the other half resulted in an altruistic outcome where both individuals received an equal reward. The individual handing the tokens to the experimenter was rewarded regardless.

If chimpanzees where choosing under a system driven by selfish interests, there should be a preference towards the choice where only the individual in control of the tokens receives a reward, and if the choice was purely random, each token would be expected to be seen 50% of the time. However, it was found that pairs where significantly more likely to share a reward (displaying prosocial behaviour), than choose the selfish option.

Victoria Hornera, J. Devyn Cartera, Malini Suchaka, and Frans B. M. de Waal (2011). Spontaneous prosocial choice by chimpanzees Proceedings of the National Academy of Sciences : 10.1073/pnas.1111088108

Moustached Tamarin (S. mystax) from The Bronx Zoo, New York City. Photo from Wikipedia.

S. mystax belong to the Callitrichid family, and like all Callitrichids has an interesting reproductive strategy unlike those of other primate families. Callitrichids form multimale-multifemale group and has a polyandrous (one female, multiple male) mating system. Callitrichids are the only primate family that consistently give birth to twins. The gestation period for S. mystax is 6 months. Usually, only one dominant female is reproductively active and shares offspring rearing responsibilities with multiple males in the group. However, an unstable dominance hierarchy among females might lead to multiple births within the group and will compromise the survivability of both the group and the offspring from stress, less parental investment and lack of food resources.

The researchers were studying how help from male moustached tamarins in the same group and the absence of female competition ensure the survival of offspring when they observed a female cannibalizing an infant. Necropsy and genetic analyses were used to rule out diseases and to determine paternity. They found that the infant has no diseases and did not die from trauma (falling from tree). Instead, it was a healthy infant and was being cannibalized by its own mother.

The mother was seen biting and then eating the head of its own infant during a period when another female was pregnant and gave birth just 1 month later. Before that, the perpetrator had given birth to twins three times successfully when four to five adult and subadult males were present in the group. Although we do not know for certain that the infant was alive when the mother started biting it, our field observations preceding the event suggest it probably was. The possible infanticide case and the two cases of births and early death of the infants occurred while only two to three adult males were present in the group. This could be the second case of maternal infanticide reported in the genus Saguinus and the similar circumstances suggest a common pattern. Culot et al. (2011).

Five common hypotheses proposed by Hrdy (1979) were used by the authors to try to explain maternal infanticide and cannibalism in this scenario. These hypotheses are resource competition, sexual selection, social pathology, exploitation, and parental manipulation.

The resource competition and sexual selection hypotheses were rejected because it was maternal infanticide, and not infanticide from another female. The social pathology hypothesis was rejected because it predicts infanticide restricted in areas that are disturbed by humans. The study group was habituated and had many successful births, therefore social pathology was ruled out. The exploitation hypothesis was also reject because the mother did not kill her infant to exploit its meat. Observation shows that the mother only consumed the brain and parts of the infant’s neck.

The parental manipulation hypothesis was accepted because the authors think that it best explains the scenario. The offspring was not pathological nor did it fell from the tree. Instead, it was a healthy infant that was killed by its own mother. According to Hrdy (1979), victim of parental manipulation does not necessarily have to be defective but also born “at the wrong place in the wrong time”.

The authors concluded that parental manipulation is the best explanation for this possible maternal infanticide scenario. Parental manipulation strategy can happen in a group with poor capacity to raise the offspring from multiple breeding females, birth intervals that are shorter than 3 months, and low infant survival probability due to physical injuries or weakness.

References:

Lingual view (side that touches the tongue) of Mescalerolemur horneri partial mandible.
Scale bar equals 2 mm. Photo from Kirk & Williams (2011).

Anywho … A fossil primate from the Eocene Epoch was discovered in Devil’s Graveyard badlands of West Texas by Anthropologists Christopher Kirk and Blythe Williams. Named Mescalerolemur horneri, this new fossil primate lived about 43 million years ago is a member of the extinct group, adapiforms, that are found all over the Northern Hemisphere. Mescalerolemur looked like a modern-day greater dwarf lemur and weighs about 370 grams.

Interestingly enough, Mescalerolemur are more closely related to Eurasian and African adapiforms than those from North America. Darwinius masillae, famously known as Aunt Ida, was a Eurasian adapiform. Another interesting fact to point out is that Mescalerolemur had unfused mandibular symphysis, similar to those of Strepsirrhines (lemurs, lorises and galagos). The authors posit that this is definitive evidence that adapiforms are more similar to Strepsirrhines than Haplorrhines (humans are Haplorrhines). Kirk &Williams (2011) published their findings on Journal of Evolution: New adapiform primate of Old World affinities from the Devil’s Graveyard Formation of Texas (PDF). You can also read more about the discovery at EurekAlert: Anthropologist discovers new fossil primate species in West Texas.

Originally posted on The Prancing Papio.