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Effects of Climate Change on Primate Evolution in the Cenozoic

By: Blythe A. Williams (Duke University) © 2016 Nature Education 
Citation: Williams, B. A. (2016) Effects of Climate Change on Primate Evolution in the Cenozoic. Nature Education Knowledge 7(1):1
Primates are smart, flexible, and adaptive creatures. How have they responded to changes in climate over millions of years?
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Japanese macaques (<em>Macaca fuscata</em>) on Mount Arashiyama, Japan.
Japanese macaques (Macaca fuscata) on Mount Arashiyama, Japan.
This species has the northern-most distribution of any living non-human primate.
Courtesy of Blythe Williams All rights reserved. View Terms of Use

Climate is the major factor that determines where a species can and cannot live. Daily and seasonal variations in temperature, annual cycles of precipitation, and larger swings in climate shape adaptations of plants and animals and ultimately may determine their survival. Changes in global and regional climates apparently had profound effects on the evolutionary history of primates. However, making direct associations between climate and evolutionary changes in morphology and behavior is difficult because the timing of environmental events relative to morphological change is often imprecise, and because factors such as interspecies competition, genetic changes, and dispersal abilities undoubtedly had critical influences as well (Behrensmeyer, 2006).

Reconstructing past environments

Many different tools can be used to reconstruct paleoenvironments. The timing and intensity of continental drift, mountain building, and rerouting of ocean circulation affect temperature and rainfall, and may impact migration routes. Stable oxygen isotopes in marine core records document past temperature shifts and modifications in glacial ice. The geological record provides information on uplift of mountain ranges and changes in the size and location of oceans (and their circulation), rivers, and lakes (Zachos et al., 2001). Transitions in rainfall patterns may be inferred from differences in the diversity and complexity observable in fossil plants. These changes in the landscape provide insights into causal factors in speciation and extinction events, and to variation in patterns of species richness (Janis, 1993).

Where do primates live today?

Modern humans live on all of the continents. Non-human primates are widespread in Africa, Asia, and South America but occupy only limited areas of Europe (Gibraltar) and North America (Central America, and southern Mexico). There is no evidence that they ever occupied Antarctica or Australia/Oceania. In the past, distributions of non-human primates extended much further north in North America and Eurasia, and further south in South America (Smith et al., 2006; Kay et al., 2008).

Most living primate species are arboreal, and it is commonly believed that primates evolved in an arboreal setting. The majority of modern primate species live in tropical and subtropical forests, as they did in the past. In the tropics, daily fluctuations in temperature are often greater than seasonal fluctuations. Seasonal fluctuations in rainfall, however, drive the distribution and diversity of vegetation, and can impact availability of resources, such as food, and other elements of habitat.

Some primates have adapted to open woodland or savanna environments. These highly seasonal environments increase exposure to predators and alter the kinds of foods available. Baboons, vervets, and patas monkeys have managed to adapt to the inherent dangers of African savannas through swift terrestrial running, heightened vigilance and social awareness. Some chimpanzee populations utilize more open woodlands, but most apes are forest dwellers. Nevertheless, our hominin ancestors adapted well to open woodlands and savannas

A few primate species have managed to colonize more temperate regions. These include the Japanese macaque (banner image), known from the northernmost latitudes of any living non-human primate, and the snub-nosed langurs of China, that live in mountainous coniferous forests. In these high-latitude temperate forest biomes, cold and snow are seasonal challenges, and primates develop thick, insulative coats. Primates find behavioral solutions to the cold such as sunning themselves on south-facing slopes, huddling together, altering their daily travel distances, and shifting their diets to take advantage of available food. No strepsirrhine is found in high latitudes and few exist at high altitudes. Their low basal metabolic rates may be a limiting factor in adapting to colder environments

Primates may be better protected from environmental change than many other animals because of their high cognitive abilities, extensive social networks, and dietary flexibility (Morris et al., 2011). Given our knowledge about the environmental preferences and requirements for living primates, what can we infer about how changing climates affected their evolutionary history?

Primate responses to environmental change

Genetic divergence dates suggest an origin for Primates in the Cretaceous (Steiper & Seiffert, 2012), however the oldest fossils that may represent the group, the plesiadapiforms or archaic primates, are first known from the Paleocene of North America, Europe, and Asia. The precise relationship of plesiadapiforms to Euprimates (true primates) is debated, though it is generally agreed that the two are part of a clade that also includes dermopterans (colugos) and scandentians (tree shrews).

Paleocene-Eocene Boundary. Marked global climatic warming occurred at the Paleocene-Eocene boundary, about 56-55 million years ago (Ma) (Paleocene-Eocene Thermal Maximum, or PETM; Figure 1). At the PETM, it has been posited that massive amounts of greenhouse gases entered the atmosphere, the source of which is unclear (Zachos et al., 2008). Major extinctions of benthic foraminifera in the oceans (Zachos et al., 2001) and terrestrial mammals coincided with these changes, and new orders of mammals emerged (Gingerich, 2006). As a result of warm climates during the Eocene, increases in plant diversity created new environmental niches favorable for primates. With the possible exception of Altiatlasius, a species from the Paleocene of Morocco, the oldest euprimates are found at the base of the Eocene. These early primates are known from China, western Europe, and North America and may have dispersed across a warm, wet, northern forest (Smith et al., 2006). Primates flourished throughout parts of North America, Europe, Asia, and Africa in the warm and humid Early and Middle Eocene, and during this time we find the first record of several major primate groups: anthropoids, adapiforms, tarsiers, and omomyiforms (Covert, 1986, 2002; Smith et al. 2006; Williams et al., 2010). They share features with living primates that are not found in plesiadapiforms, including large, convergent orbits with a bony bar on the lateral rims. These and other cranial features indicate an increasing reliance on vision rather than smell or tactile senses, and may have evolved in association with insect predation in low light environments such as the canopies and understories of tropical forests (Cartmill, 1992; Ravosa & Savakova, 2004). Many of these early primates were extremely small, some of them smaller than any primates living today (Gebo, 2004). All known taxa display postcranial adaptations suggesting arboreality and many appear to have used leaping to bridge gaps in the forest (Covert, 1986).

Fluctuations in global climate during the Cenozoic.
Figure 1: Fluctuations in global climate during the Cenozoic.
The curve (red line) was generated from data published by Zachos et al. (2008), and is a record of δ18O (the ratio between oxygen-18 and oxygen-16 isotopes) in samples of deep-sea benthic foraminifera. The temperature scale on the left only applies to the period of time before the development of the Antarctic ice sheets (about 35 Ma) because the volume of water stored in ice affects the isotopic ratio. Date for Plio-Pleistocene boundary is debated in the literature. Bars for ice sheets: black is full scale and permanent, gray is partial or ephemeral. Example shown of deep-sea benthic foraminifer Planulina wuellerstorfi, scanning electron micrograph courtesy of Bruce Corliss (unpublished SEM); breadth equals ~400μm.
Courtesy of Blythe Williams All rights reserved. View Terms of Use

In the Middle to Late Eocene, North America experienced mountain building and drying trends which turned the humid subtropical forests into seasonally drier forests. These climatic changes were apparently catastrophic for primates, which were virtually extinct in North America by the Late Eocene (Williams & Kirk, 2008).

Eocene-Oligocene Boundary. Throughout much of the early Cenozoic, the polar regions had little to no ice. Concentrations of greenhouse gases, and thus mean global temperatures, were much higher than today. Beginning about 50 Ma, Earth began a long-term cooling (Zachos et al., 2008). Collision of the Indian tectonic plate with the Asian plate and consequent uplift of the Tibetan plateau, beginning about 55 Ma, may have resulted in increased weathering rates, hence decreased atmospheric CO2 concentrations and cooler temperatures (Raymo & Ruddiman, 1992). Further global cooling occurred between about 34-33 Ma (Zachos et al., 2001), just after the Eocene-Oligocene Boundary (EOB), associated with changing positions of continents and alterations in ocean circulation due to the opening of some ocean gateways and closing of others. There was growth of the Antarctic ice sheet and the beginnings of the "icehouse" conditions that exist today (Katz et al. 2008; Zachos et al., 2001). Cooler temperatures are associated with the retreat of subtropical forests and a large-scale mammalian turnover in North America, Europe (where it is called the Grande Coupure), and Asia (where it is called the Mongolian Remodeling). Just a few primate taxa survived the Grande Coupure in Europe (Hooker et al, 2004; Meng and McKenna, 1998; Zanazzi et al., 2007).

Tropical South India, Southeast Asia, and presumably equatorial Africa and Madagascar would have served as refugia for primates during the Oligocene. Parts of Afro-Arabia also supported primates during the Oligocene. Dozens of fossil primate species are known from North Africa, including adapiforms, anthropoids, and fossil lorises and galagids. During the Late Eocene and Early Oligocene, parts of this area were warm, wet, seasonal forests influenced by monsoons. Several strepsirrhine groups disappear around the EOB in North Africa, while anthropoids continued to diversify into the Early Oligocene (Seiffert, 2007). Primates appear in South America for the first time in the Late Oligocene, at 26 Ma (Kay et al., 2002), and it is hypothesized that the ancestor to modern platyrrhines (New World monkeys) migrated from Africa during a period of low sea level, across Atlantic Ocean ridges or series of islands which may have been exposed, and eventually expanded throughout South and Central America and into southern North America (Fleagle & Kay, 1997).

Oligocene-Miocene emergence of Old World Monkeys and Apes. Toward the end of the Oligocene and into the Early and Middle Miocene, there was a warming trend, expansion of subtropical forests, and a diversification of catarrhine primates in Africa and the Arabian Pensinsula (Harrison, 2002; McNulty, 2010). Non-cercopithecoid catarrhine primates were diverse in the Early and Middle Miocene of Africa. Beginning around 17 Ma they spread to Eurasia via a landbridge that formed across the Tethys Sea as a result of continental collisions, and led to the separation of the Arabian Gulf and the eastern Mediterranean (Rögl, 1999, Harrison, 2010). Undisputed members of the Hominoidea, the modern ape radiation, appeared and diversified in Africa and Eurasia during a period of global warming (the Mid-Miocene Climatic Optimum) and forest expansion (Begun, 2002; Harrison, 2010; Kelley, 2002; McNulty, 2010). Most living apes are heavily dependent on trees for under-branch suspensory locomotion, foraging, and nest building, and live in tropical forests with low seasonality. If their extinct relatives were similar, the conditions during this time period would have been ideal. Old World monkeys (cercopithecoids) were rare until late in the Miocene when seasonality began to increase, and vegetation north of the Tropic of Cancer shifted from subtropical evergreen to deciduous woodlands. Their success in this more seasonal environment may be due to the broad scope of their diets, their accelerated (relative to apes) life history (i.e., early reproduction and short periods of gestation, weaning, and interbirth intervals), and flexible locomotor patterns that allowed them to move easily in trees and on the ground (Jablonski, 2005). Cercopithecoids radiated throughout Africa and Eurasia into the Pliocene and Pleistocene and continue to be extremely successful today.

The increase in seasonality and loss of evergreen forest habitats was disastrous for apes. At about 9.6 Ma, most apes disappeared from Eurasia, as did other mammals dependent on forests. This extinction event in Europe is referred to as the Vallesian Crisis (Agustí et al., 2003; Begun et al., 2012). Some surviving apes developed thick dental enamel and low crowned teeth - features suggesting a diet of hard, abrasive food items such as seeds and nuts that might have been available in open semi-arid habitats. However, by the end of the Miocene, few dense forests remained and Eurasian hominoids were restricted to their present distribution in the tropical forests of Southeast Asia and southern China (Harrison, 2010; Begun et al, 2012).

Emergence of hominins in the Pliocene. Cooling and drying continued into the Pliocene, and grasslands expanded (Bobe and Behrensmeyer, 2004). From about 8-6 Ma there was a global increase in the dominance of C4 grasses (Cerling et al. 1997), indicative of hotter and drier climates. Fossils that may represent early bipedal hominins appear in Africa between 7 and 4 Ma, some from environments that were forested and others from more arid environments. It is not clear if either of these environments selected for bipedalism.

The availability and exploitation of C4 foods (tropical grasses, sedges, and animals that eat these plants) may have implications for the diets of early human ancestors and other early hominins. The consumption of C4 foods leaves a record in developing dental enamel that can be identified through the study of stable carbon isotopes (Cerling et al., 1997). Extant apes use few, if any, C4 foods in their diets, even those living in open, woodland environments where these foods are readily available. However, some early hominins apparently specialized in such foods. The shift away from reliance on C3 plants such as hard fruits and nuts and the increase in consumption of C4 foods signals the expansion of early hominins into drier habitats, and the ability to tolerate fluctuations in climate that would otherwise have severely limited the availability of food items (Lee-Thorpe et al., 2010). By about 2 Ma, at least one species of the genus Homo became a much faster runner and efficient hunter, and was able to exploit the open grasslands of Africa (Bramble and Lieberman, 2004). Expansion of grasslands and open habitats may also have contributed to diversification of cercopithecoids in southern Africa (Elton, 2007).

By 1.8 Ma, hominins had expanded their range beyond the tropics of Africa and into more variable environments of Asia where they encountered new extremes of temperature and types of vegetation. There was substantial environmental instability in the Pliocene and Pleistocene (Zachos et al., 2008), as temperatures and rainfall fluctuated dramatically, especially after about 700,000 years ago. Significant faunal turnover in Africa occurred at about that time. This environmental instability may have selected for hominins with larger brains capable of developing flexible coping strategies, new technologies (such as lithic tools), and more complex social networks (Potts, 1996; 2007).

Islands in the Holocene. High sea levels may have been responsible for a number of extinctions among primates during the Holocene, including a large rise in sea levels that occurred at about 10,000 years ago. Primates on small islands were probably especially susceptible to extinction. It is likely that environmental degradation due to human activities contributed to the widespread extinction of primates in Madagascar and island primates in the Caribbean during the Holocene (Morgan and Woods, 1986).


Adapiformes (adapiforms) - a clade of primates known from the Eocene-Miocene, which may represent stem strepsirrhines

Anthropoidea (anthropoids) - a clade consisting of living monkeys and apes plus their extinct relatives

arboreal - living in trees

benthic foraminifera - single-celled organisms that dwell in the sediment of the ocean floor

Catarrhini (catarrhines) - a clade of Old World monkeys and apes plus their extinct relatives

Cercopithecoidea (cercopithecoids) - a clade of living Old World monkeys and their extinct relatives

clade - a group consisting of an ancestor and all of the descendant branches from than ancestor

Cretaceous - a geologic period from ~145.5 to ~65.5 million years ago

Eocene - a geologic epoch from ~55.8 to ~33.9 million years ago

Euprimates (true primates) - a clade of living primates (lemurs, lorises, galagos, tarsiers, platyrrhines, and catarrrhines), extinct omomyiforms and adapiforms, and all extinct species that are more closely related to this clade than they are to its sister groups Scandentia (tree shrews), Dermoptera (colugos), and the extinct plesiadapiforms

grande coupure and Mongolian remodeling - sudden, major changes in the terrestrial fauna of Europe (grande coupure) and Asia (mongolian remodeling) that took place ~34 million years ago, associated with dramatic cooling of global climate

Haplorhini (haplorhines) - a clade of living primates that includes tarsiers, platyrrhines, and catarrhines plus their extinct relatives

Holocene - a geologic epoch from ~11.7 thousand years ago to the present

Hominini (hominins) - a clade that includes living and fossil humans

Homo - a genus that includes modern humans (Homo sapiens) plus the most closely related fossil human species

Hominoidea (hominoids) - a clade of living apes (gibbons, siamangs, orangutans, gorillas, chimpanzees, bonobos, and humans) plus their extinct relatives

Miocene - a geologic epoch from ~23 to ~5.3 million years ago

Mongolian remodeling - see grande coupure

Oligocene - a geologic epoch from ~33.9 to ~23 million years ago

Omomyiformes (omomyiforms) - a clade of primates, known primarily from the Eocene, which might be closely related to tarsiers and anthropoids

Paleocene - a geologic epoch from ~65.5 to ~55.8 million years ago

Pliocene - a geologic epoch from ~5.3 to ~2.6 million years ago

Pleistocene - a geologic epoch from ~2.6 Ma to ~11.7 thousand years ago

Plio-Pleistocene - specifically refers to the Pliocene and Pleistocene epochs together, from ~5.3 million to ~11.7 thousand years ago, but sometimes also includes the Holocene (from the end of the Pleistocene to the present)

Platyrrhini (platyrrhines) - a clade of living New World monkeys from Central and South America, and their extinct relatives

speciation - the splitting of a lineage into two or more separate species

species richness - the number of species represented in a given area

stable oxygen isotopes - different variants of the element oxygen that are not radioactive, i.e., they do not decay into other elements. The three stable isotopes in naturally occurring oxygen are 16O, 17O, and 18O. The ratio of 18O to 16O in ice cores, marine sediments, and fossils is used for identifying warmer or cooler periods in the past. Greater abundance of the lighter weight 16O (8 protons, 8 neutrons) is indicative of warmer periods whereas greater abundance of the heavier weight 18O (8 protons, 10 neutrons) is indicative of cooler periods.

Strepsirrhini (strepsirrhines) - a clade of living lemurs, lorises, and galagos and their extinct relatives

tarsiers - small-bodied, nocturnal, insectivorous primates living today in Southeast Asia, and known from fossils in other parts of Asia. Tarsiers are the living sister-group of anthropoids.

Vallesian Crisis (or Mid-Vallesian Crisis) - a land mammal extinction event that occurred 9.5 million years ago in Eurasia, and is associated with cooling and drying, and widespread changes in vegetation.


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