Morphological innovation, diversification and invasion of a new adaptive zone

Abstract

How ecological opportunity relates to diversification is a central question in evolutionary biology. However, there are few empirical examples of how ecological opportunity and morphological innovation open new adaptive zones, and promote diversification. We analyse data on diet, skull morphology and bite performance, and relate these traits to diversification rates throughout the evolutionary history of an ecologically diverse family of mammals (Chiroptera: Phyllostomidae). We found a significant increase in diversification rate driven by increased speciation at the most recent common ancestor of the predominantly frugivorous subfamily Stenodermatinae. The evolution of diet was associated with skull morphology, and morphology was tightly coupled with biting performance, linking phenotype to new niches through performance. Following the increase in speciation rate, the rate of morphological evolution slowed, while the rate of evolution in diet increased. This pattern suggests that morphology stabilized, and niches within the new adaptive zone of frugivory were filled rapidly, after the evolution of a new cranial phenotype that resulted in a certain level of mechanical efficiency. The tree-wide speciation rate increased non linearly with a more frugivorous diet, and was highest at measures of skull morphology associated with morphological extremes, including the most derived Stenodermatines. These results show that a novel stenodermatine skull phenotype played a central role in the evolution of frugivory and increasing speciation within phyllostomids.

Figure 1.

Summary phylogeny of 150 species of phyllostomid bats illustrating diversity in lineages and morphology among subfamilies. Branch lengths are proportional to time and grey bars indicate 95% confidence intervals (CI) around node dates. The yellow arrow indicates the node where the largest shift in species diversification rate was found. Clockwise from top species are: Lonchorhina aurita, Lonchophylla robusta, Musonycteris harrisoni, Glyphonycteris silvestris, Carollia castanea, Sturnira lilium, Sphaeronycteris toxophyllum, Artibeus jamaicensis, Uroderma bilobatum Vampyressa pusilla, Platyrrhinus umbratus, Noctilio albiventris (outgroup), Micronycteris hirsuta, Desmodus rotundus, Lophostoma silvicolum.

Figure 2.

Frequency distributions derived from analyses of 1000 phylogenies. (a) MCMC sampling of birth rates across whole phylogenies, (b) rates of evolution of PC1 and (c) ln trophic level for the Phyllostomidae (black bars) as a whole, the subfamily Sternodermatinae (dark grey bars) and non-stenodermatine (light grey bars) phyllostomids.

Figure 3.

PC1 as a predictor of ln trophic level (a, mean coefficient = 0.193 ± 0.015) and ln bite force (b, mean coefficient = −0.327 ± 0.007). Symbols represent species means, and the size of the symbols indicate the magnitude of the significant, independent contributions of PC2 to ln trophic level (a, mean coefficient = −0.081 ± 0.015) and ln head height to ln bite force (b, mean coefficient = 2.826 ± 0.034). The relationships were modelled using GLS fitted with ML and phylogeny-based correlation structures of the errors. The relationship between skull morphology and PC1 scores are illustrated from left to right by: Centurio senex, Carollia perspicillata, Phyllostomus elongatus, Micronycteris hirsuta, Choeronycteris mexicana.

Figure 4.

Best-fit models of speciation as a function of trait evolution for 100 phylogenies. (a) Ln trophic level: (i) nonlinear model (mean highest speciation rate: 0.409 ± 0.028 attained at −0.030 ± 0.011 on the ln trophic level axis; mean lowest speciation rate: 0.118 ± 0.008); and (ii) linear model (mean intercept speciation rate: 0.263 ± 0.016, mean coefficient speciation rate on ln trophic level: −0.311 ± 0.023). (b) PC1: (i) nonlinear model (mean lowest speciation rate: 0.038 ± 0.020 attained at 0.442 ± 0.154 on the PC1 axis; mean highest speciation rate: 0.424 ± 0.223); and (ii) linear model (mean intercept speciation rate: 0.122 ± 0.016, mean coefficient speciation rate on ln trophic level: −0.048 ± 0.005). Observed trait values are shown as ticks on the x-axes.