Iterative adaptive radiations of fossil canids show no evidence for diversity-dependent trait evolution

A long-standing hypothesis in adaptive radiation theory is that ecological opportunity constrains rates of phenotypic evolution, generating a burst of morphological disparity early in clade history. Empirical support for the early burst model is rare in comparative data, however. One possible reason for this lack of support is that most phylogenetic tests have focused on extant clades, neglecting information from fossil taxa. Here, I test for the expected signature of adaptive radiation using the outstanding 40-My fossil record of North American canids. Models implying time- and diversity-dependent rates of morphological evolution are strongly rejected for two ecologically important traits, body size and grinding area of the molar teeth. Instead, Ornstein–Uhlenbeck processes implying repeated, and sometimes rapid, attraction to distinct dietary adaptive peaks receive substantial support. Diversity-dependent rates of morphological evolution seem uncommon in clades, such as canids, that exhibit a pattern of replicated adaptive radiation. Instead, these clades might best be thought of as deterministic radiations in constrained Simpsonian subzones of a major adaptive zone. Support for adaptive peak models may be diagnostic of subzonal radiations. It remains to be seen whether early burst or ecological opportunity models can explain broader adaptive radiations, such as the evolution of higher taxa.A central prediction of modern adaptive radiation theory is that rates of diversification and phenotypic evolution are fastest early in clade history and subsequently slow as niches become saturated (1). This prediction is derived in large part from the writings of Simpson (2, 3), who suggested that fast rates of phenotypic evolution are required during the early phases of adaptive radiation to move lineages rapidly through inadaptive phases of the adaptive landscape to a new peak. Although the fossil record provides many examples of rapid early accumulation of morphological disparity (4–10), direct evidence for early rapid rates of phenotypic evolution, a so-called “early burst,” has proved rare in phylogenetic comparative data (11). There are several plausible explanations for why early bursts are seldom observed. For example, temporally declining rates are difficult to detect in datasets comprising only extant taxa, and comparative methods are extremely sensitive to noise from convergence or measurement error (11, 12). Incorporation of fossil taxa in phylogenetic tests for early bursts can improve detection of these patterns (13), although isolated analyses of subclades within a larger adaptive radiation may fail to show evidence of declining disparity with time if rates have already significantly decreased, even when fossil species are sampled (14).An alternative explanation for the lack of early bursts in comparative data is that ecological opportunity, not time, is the key determinant of rates of morphological evolution. If opportunity is the dominant force driving rates of morphological evolution in adaptive radiation, then the early burst model should be a particularly poor fit when clade age is a weak predictor of species richness. Patterns of diversity through time in the fossil record strongly suggest that diversity-dependent speciation and extinction dynamics are common (15–17) and weak or negative relationships between clade age and species richness are increasingly recognized in molecular phylogenies (18–20). To test the role of ecological opportunity in driving the morphological component of adaptive radiation more explicitly, Mahler et al. (21) developed a novel approach to model rates of morphological evolution as function of estimated past diversity at nodes of a time-calibrated molecular phylogeny (a similar method can be found in ref. 22). Using estimated lineage diversity as a proxy for past ecological opportunity in island communities of Anolis lizards, they found strong support for diversity dependence of evolutionary rates for body size and limb bone lengths, both of which influence habitat use and performance (21). This result would seem to lend support to a primary role for ecological opportunity in regulating rates of morphological evolution during adaptive radiation. It remains to be tested, however, whether diversity dependence can provide a compelling mechanism to explain patterns of morphological disparity through time in more general contexts, such as on continents, or over longer geological times scales.In this article, I test for diversity dependence of rates of body size and dental evolution in living and fossil members of the dog family, Canidae. Canids are an attractive system for such a study. Living canids exhibit a range of dietary and predatory behaviors that can be readily diagnosed for fossil species on the basis of craniodental traits (23, 24). The canid fossil record is also well sampled, yielding a diverse radiation of ∼140 species (25–27) that spans the Late Eocene (40 Mya) through present day. Perhaps most importantly, however, for the first 35 My of their evolutionary history, canids were restricted to and diversified exclusively within North America. If ecological opportunity plays a prominent role in regulating rates of morphological diversification over geological time scales, we should expect to find support for a link between diversity and the tempo of ecomorphological diversification in continental radiations with excellent fossil records, such as Canidae.