Primate diversification inferred from phylogenies and fossils

Abstract

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ∼600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ∼34 Ma, but also elevated extinction ∼10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.

Reevaluating cases of trait‐dependent diversification in primates

“…There are at least two factors that misled previous SSE analyses of frugivory, mutualism, and terrestriality. The first is the high rate of diversification found in Cercopithecoidea relative to other primates (Arbour & Santana, ; Fabre et al, ; FitzJohn, ; Herrera, ; Paradis, ; Purvis, Nee, & Harvey, ; also replicated here—see Fig. and Fig.…”

“…The very high rate of diversification in cercopithecoids relative to other primate clades is a well‐established feature of primate macroevolutionary studies (Arbour & Santana, ; Fabre et al, ; FitzJohn, ; Herrera, ; Paradis, ; Purvis, Nee, & Harvey, ; Springer et al, ). Various aspects of cercopithecoid biology have been invoked to explain their recent evolutionary success, especially relative to the Hominoidea—their extant sister clade and primary ecological competitor.…”

“…Random events, climatic trends and fluctuations, biogeographic histories, and interspecific interactions, both within and outside of the order, are all thought to have played important roles in shaping primate phylogeny (Fleagle, ; Kamilar & Beaudrot, ; Lehman & Fleagle, ; Reed & Bidner, ). In addition, the fossil record reveals a number of episodes of patterned extinction: whole groups have been lost (e.g., Adapiformes and Omomyiformes) and some of the crown clades have suffered recent dramatic declines in biodiversity (e.g., Hominoidea) (Fleagle, ; Herrera, ; Springer et al, ). Given the complexity of primate evolutionary history, detecting trait‐dependent diversification and distinguishing its effects from the effects of other factors is challenging.…”

“…Greater vulnerability of diurnal species to extinction combined with entrenched nocturnal mammalian diversity may explain the pattern detected in the present study. That is, the higher rates of net diversification in diurnal primates may reflect a boom‐bust cycle, with primates being one of the first crown groups of mammals to become established in the diurnal arboreal niche, suffering heavy losses during periods of climatic cooling (Herrera, ; Springer et al, ), and then rebounding or reinvading the niche, whereas nocturnal primate diversity was less volatile. The higher speciation and extinction rates estimated for diurnal lineages by the BiSSE and HiSSE models using the broad‐ and narrow‐sense schemes are consistent with this idea (Table ).…”

“…That SSE methods can be misled by trait‐independent variation in diversification rates represents a problem for primates. Studies that have examined how diversification varies among primate clades have consistently detected rate heterogeneity, with the most common result being an elevated rate among cercopithecoids relative to other groups (Arbour & Santana, ; Fabre, Rodrigues, & Douzery, ; FitzJohn, ; Herrera, ; Paradis, ; Purvis, Nee, & Harvey, ). While this pattern might be driven by one or more of the traits considered in previous investigations, other factors have not been ruled out.…”