"Rise of the continent of the monkeys": an integrated genomic and fossil-based analysis of the adaptive radiation of New World primates

New World primates live in the tropical regions of Central and South America, and include such well-known and charismatic species as spider monkeys, howler monkeys, marmosets and capuchins. Today, there are more than 170 species known in five families, which collectively exhibit a broad range of different body sizes, diets and activity. Remarkably, all this diversity originated from a single common ancestor that reached South America from Africa 35-45 million years ago, probably by being transported over sea on a raft of vegetation. Why and how did this ancestor give rise to all the varied species that make up modern New World primate radiation? What were the drivers leading to the diversification of the different families? Were abiotic factors like changes in climate, the uplift of the Andes mountains, and the development of the Amazon river, or were biotic factors (competition with other mammals) more important in driving diversification? Can we identify when and why there were changes in body size, diet and activity pattern in different New World primate groups? Our proposed project will attempt to answer these questions. To do so, we will combine two very different, but complementary, types of data: genomic data, which provides detailed information on living species, and fossil data, which provides (often very incomplete) information on past diversity. Previous studies have usually used either genomic data or fossil data, but ours will combine the two, to take advantage of their different strengths and to compensate for each other's weaknesses.
Firstly, we will examine the genomes of different New World primate species to see if we can identify genes relating to traits like diet, body size and activity pattern. By doing so, we will be able to infer how these traits have changed through time in the different New World primate groups. Secondly we will produce a new evolutionary tree (phylogeny) of all the living New World primate species, using large amounts of genomic data and sophisticated methods to produce the most complete and accurate phylogeny of the group, and we will use "molecular clocks" to infer divergence times for when different lineages split from one another. With our new phylogeny and divergence times, we will examine how the rate of diversification has varied through time, and whether very high or low rates of diversification coincide with periods of environmental change. We will also identify previously unrecognised species and reassess the taxonomy of all known species. This information will be key to conservation efforts, by helping identify the species most in need of protection to conserve maximum biodiversity.
Thirdly, we will use data from the fossil record to model how living and extinct lineages of New World primates have diversified through time. This data can be compared with the pattern of diversification indicated by the phylogeny of living New World primates, to see if they are broadly similar. If they show major differences, this suggests that extinction has played a key role in New World primate evolution. We will also use the fossil record to test the hypothesis that New World primates outcompeted superficially "primate-like" mammals (actually, relatives of modern marsupials) that were already present in South America when the New World primate ancestor arrived from Africa.
Our project will massively increase our understanding of New World primate evolution, shed new light on diversification and evolutionary processes in general, and help identify those New World primates most vulnerable to extinction. In doing so our findings will be of interest to a wide range of scientists, including evolutionary biologists, genomicists, ecologists and palaeontologists. Because our project, by rigorously clarifying NWP species numbers and boundaries, our results will also have broader practical utility for conservation practitioners and policy makers in governmental and non-governmental agencies.

The >170 species of New World primates comprise ~10% of total Neotropical mammal biodiversity. 45% of these are threatened, with 10% critically endangered. In order to protect this remarkable group, an accurate understanding of its diversity is essential. However, the description of new species (30 since 1990) has forced government and non-governmental agencies to repeatedly reassess species threat status and modify conservation strategies and action plans, at considerable financial cost. A major outcome of our project will be an accurate, stable species-level taxonomy of New World primates that will facilitate threat assessments, and aid conservation and development planning. The main likely beneficiaries are:

POLICY-MAKERS: The UN's 2010 Convention of Biological Diversity (CBD) states that biodiversity is "a common concern to humankind'. >100 countries have signed the 2011-2020 Global Biodiversity Strategic Plan, which states that 'Biodiversity underpins ecosystem functioning and the provision of ecosystem services essential for human well-being...and is essential for the achievement of the Millennium Development Goals, including poverty reduction'. Target 19 of the CBD strategic plan states that 'biodiversity knowledge worldwide should be improved...widely shared and transferred, and applied''. The main indicator of this target is the Global Biodiversity Information Facility (GBIF) database. Our project will allow us to correctly identify all >400 tissue samples collected by CI Boubli and additional samples from project partners to species level. We will enter this information and associated locality data into GBIF, and into other open-access biodiversity databases (e.g. GEOSS, Specieslink) that policy-makers use to inform decision-making regarding biodiversity.

CONSERVATION PRACTITIONERS: require accurate, up-to-date species-level taxonomies and species locality data, in order to identify species and determine their geographical distributions. This allows their threat status and need for protection to be assessed and monitored. Particularly important is the IUCN Red List, which is used by conservation practitioners and which is also an indicator for the CBD's Target 12 ('Preventing Extinctions') and for WWF's Living Planet Index. Captive breeding programmes in zoos also require accurate species delimitation, to identify target species and to ensure their genetic integrity. CI Boubli is a member of the IUCN's Primate Specialist Group, which prepares threat assessments used in the ICUN Red List; Boubli will directly incorporate data from this project (namely the revised species list and associated locality data) into future threat assessments. This data will also be made available via relevant open-access databases (GBIF, GEOSS, Specieslink) for direct use by conservation practitioners.

DEVELOPMENT AGENCIES: Growth of Latin American economies is leading to rapid advancement of the agricultural frontier and infrastructure projects (e.g. dams in Amazonia). Accurate characterisation of biodiversity is needed to enable decision makers to minimise environmental impact (e.g. by avoiding high impact development activities in diversity "hotspots") and better offset their impact activities. As above, our data regarding species identity and locality data for New World primate species will be made available via open-access databases (GBIF, GEOSS, Specieslink) for use in development planning.

GENERAL PUBLIC AND MEDIA: New World primates are a well-known, charismatic group. Forms such as spider monkeys and howler monkeys are familiar to the general public, and so our project will be of broad non-specialist appeal. The discovery of new mammal species generates considerable public and media interest (cf. description of the "olinguito" in 2013). To maximum public engagement, we will hold an outreach event in Year 2 presenting the results of our project at Manchester Science Festival (see Pathways to Impact).