Modeling lineage and phenotypic diversification in the New World monkey (Platyrrhini, Primates) radiation

Highlights

• We estimate a dated platyrrhine phylogenetic tree for ca. 80% extant species.

• Extant lineage diversification shows a constant rate of accumulation.

• In contrast, body size diversification shows a pattern of early niche partition followed by stasis.

• Body size evolved according to the occupation of a multidimensional niche.

• When oldest fossils are included, an early pulse of lineage origination appears.

Abstract

Adaptive radiations that have taken place in the distant past can now be more thoroughly studied with the availability of large molecular phylogenies and comparative data drawn from extant and fossil species. Platyrrhines are a good example of a major mammalian evolutionary radiation confined to a single continent, involving a relatively large temporal scale and documented by a relatively small but informative fossil record. Here, we present comparative evidence using data on extant and fossil species to explore alternative evolutionary models in an effort to better understand the process of platyrrhine lineage and phenotypic diversification. Specifically, we compare the likelihood of null models of lineage and phenotypic diversification versus various models of adaptive evolution. Moreover, we statistically explore the main ecological dimension behind the platyrrhine diversification. Contrary to the previous proposals, our study did not find evidence of a rapid lineage accumulation in the phylogenetic tree of extant platyrrhine species. However, the fossil-based diversity curve seems to show a slowdown in diversification rates toward present times. This also suggests an early high rate of extinction among lineages within crown Platyrrhini. Finally, our analyses support the hypothesis that the platyrrhine phenotypic diversification appears to be characterized by an early and profound differentiation in body size related to a multidimensional niche model, followed by little subsequent change (i.e., stasis).

Introduction

The study of lineage and phenotypic diversification in living clades with relatively recent divergences has supported models of adaptive radiation (Simpson, 1953, Schluter, 2000) that predict selective influences arising from ecological opportunity and circumstances (Gavrilets and Losos, 2009, Losos and Mahler, 2010). This process frequently results in great phenotypic variation and species richness relative to a short time frame of phylogenetic divergence (Schluter, 2000, Gavrilets and Losos, 2009, Losos and Mahler, 2010). It is also suspected that similar processes of adaptive radiation have driven the initial diversification of clades that originated in the distant past, for example, at the ordinal and subordinal levels in mammalian clades (Gavrilets and Losos, 2009, Losos and Mahler, 2010). In such cases, ecological opportunity may decrease during the radiation as niches are filled, leading to stasis.

Several evolutionary radiations have been carefully studied with recently developed mathematical models applied to molecular phylogenies and comparative data from extant species (Nee, 2006, Gavrilets and Losos, 2009, Losos and Mahler, 2010). However, it is becoming clear that our capacity to successfully model and understand the diversification processes of ancient clades is limited when only neontological data are considered (Quental and Marshall, 2010, Slater et al., 2012). New World monkeys (Parvorder Platyrrhini), one of the three major groups of living and fossil primates, are a good example of a major mammalian evolutionary radiation that occupies a large temporal scale (i.e., 20–40 million years ago or megannums [Ma] in Central and South America), exhibits a remarkable phenotypic variation (e.g., a body mass spanning two orders of magnitude, from 0.1 to more than 10 kg) and presents a relatively small but informative fossil record (Fleagle, 1999, Fleagle and Tejedor, 2002, r, 2008). Morphological and phylogenetic studies have hypothesized that the diversification of this monophyletic group was mainly linked to the action of deterministic-selective factors related to ecological variables (Rosenberger, 1992, Marroig and Cheverud, 2001, Rosenberger et al., 2009). However, there is no general agreement about the main ecological dimension—e.g., diet, locomotion or a multidimensional niche—behind the platyrrhine diversification (Rosenberger, 1992; Allen and Kay, 2012; Youlatos and Meldrum, 2011; Perez et al., 2011). It has also been suggested that the marked phenotypic diversification of platyrrhines occurred relatively quickly during the initial branching process of the main extant clades in connection with ecological niche opportunity (i.e., an early-burst platyrrhine radiation), followed by a slowdown in evolutionary rates which resulted in the widespread retention of the formative patterns that are characteristic of these lineages (i.e., evolutionary stasis; Rosenberger, 1992, Rosenberger et al., 2009, Perez et al., 2011).

Although some recent studies of evolutionary radiations have included information from the fossil record along with phylogenies and comparative data of extant species in a mathematical modeling framework (Slater et al., 2010, Slater et al., 2012, Etienne et al., 2011), such approach to the study of the dynamic processes of lineage origin and extinction, and phenotypic diversification, has not been applied to explore the platyrrhine evolutionary radiation. Here, we present comparative evidence using data on extant and fossil species to explore alternative evolutionary models in an effort to better understand the process of platyrrhine lineage and phenotypic diversification. Specifically, we compare the likelihood of null models of lineages and phenotypic diversification versus various models of adaptive evolution. Moreover, we explore the main ecological dimension behind the platyrrhine diversification. If the platyrrhine diversification conforms to the adaptive radiation theory, we expect that differentiation of the major extant platyrrhine lineages was concentrated relatively early in the history of the clade and that phenotypic variation—measured as body size—was partitioned among subclades early in their phylogenetic history as well, as a major driver or consequence of ecological niche partitioning and niche-filling. As a starting point, we first estimate a chronophylogenetic tree for most extant platyrrhine species using molecular data and Bayesian methods (Drummond et al., 2006). Then, using this tree and comparative statistical methods we explore the pattern of lineage diversification through time (Nee et al., 1992, Harmon et al., 2003, Ricklefs, 2007, Stadler, 2011a), investigate the pattern of body size diversification through time and the fit of a series of evolutionary models (Harmon et al., 2003, Butler and King, 2004). Finally, given that the inference of the tempo and mode of diversification of a clade using only extant species can be biased (Quental and Marshall, 2010, Slater et al., 2012), we compare the results based on extant species with the estimated body masses and number of lineages inferred from the platyrrhine fossil record. Summarizing, our work contributes to the discussion of platyrrhine evolution and diversification in three different ways: (1) we present one of the most complete molecular phylogenies of extant platyrrhine species to date, sampling published data on 108 taxa and estimating a chronophylogenetic tree for 78 putative “good” species; (2) we mathematically model the pattern of lineage and phenotypic diversification of the platyrrhine clade; and (3) we combine data about extant and fossil species in a novel way not employed before in studies of the platyrrhines to better understand the process of their diversification.