On the cusp of adaptive change: the hierarchical radiation of phyllostomid bats

Abstract

Adaptive radiations are bursts in biodiversity that lead to the origin of new evolutionary lineages and phenotypes. However, adaptive radiations typically occur over millions of years and it is unclear how the macroevolutionary dynamics that underpin them vary through time and among groups of organisms. Phyllostomid bats radiated extensively for diverse diets -from insects to vertebrates, fruit, nectar, and blood- and we use their molars as a model system to examine the dynamics of adaptive radiations. Three-dimensional shape analyses of lower molars of Noctilionoidea (Phyllostomidae and close relatives) indicate that different diet groups exhibit distinct morphotypes. Comparative analyses further reveal that phyllostomids are a striking example of a hierarchical radiation; their initial, higher-level diversification involved an early burst in molar morphological disparity as lineages invaded new diet-affiliated adaptive zones, followed by subsequent lower-level diversifications within adaptive zones involving less dramatic morphological changes. We posit that strong selective pressures related to initial shifts to derived diets may have freed molars from morpho-functional constraints associated with the ancestral molar morphotype. Then, lineages with derived diets (frugivores and nectarivores) diversified considerably within broad adaptive zones, likely reflecting finer-scale niche partitioning. The observed early burst pattern is only evident when examining molar traits that are strongly linked to diet, highlighting the importance of ecomorphological traits in comparative studies. Our results support the hypothesis that adaptive radiations are commonly hierarchical and involve different tempos and modes at different phylogenetic scales, with early bursts being more common at broader scales. SIGNIFICANCE STATEMENTMany groups of organisms are exceptionally diverse in their ecology, morphology, and number of species. But there is debate as to whether these groups commonly achieved this diversity through bursts in diversification early in their history. Phyllostomid bats are one of the most ecologically diverse mammalian families and a classic example of an adaptive radiation. We use their molar shapes, which correlate with diet, as a model for examining macroevolutionary patterns during diversifications. We find that phyllostomids experienced a two-step process of diversification; the first step involved a rapid burst, whereas the second involved finer-scale changes as lineages filled ecological niches. We posit that this is a common, yet underappreciated, pattern during the early histories of many diverse clades.