Miocene biome turnover drove conservative body size evolution across Australian vertebrates

Abstract

On deep time scales, changing climatic trends can have a predictable influence on macroevolution. From evidence of mass extinctions, we know that rapid climatic oscillations can indirectly open niche space and precipitate adaptive radiation, changing the course of ecological diversification. These dramatic shifts in the global climate, however, are rare events relative to extended periods of protracted climate change and biome turnover. It remains unclear whether during gradually changing periods, shifting habitats may instead promote non-adaptive speciation by facilitating allopatry and phenotypic conservatism. Using fossil-calibrated, species-level phylogenies for five Australian radiations comprising more than 800 species, we investigated temporal trends in biogeography and body size evolution. Here, we demonstrate that gradual Miocene cooling and aridification correlates with the restricted phenotypic diversification of multiple ecologically diverse vertebrate groups. This probably occurred as species ranges became fractured and isolated during continental biome restructuring, encouraging a shift towards conservatism in body size evolution. Our results provide further evidence that abiotic changes, not only biotic interactions, may act as selective forces influencing phenotypic macroevolution.

Keywords: adaptive radiation; comparative methods; macroevolution; marsupials; phenotypic evolution; reptiles.

Figure 1.

Shifts in evolutionary mode (BM to OU) of body size evolution are temporally clustered in the Late Miocene and congruent with a shift in dispersal histories. (a) Dotted vertical lines and density distributions are colour-coded by clade and indicate crown divergences and inferred shift timing of each focal radiation. Shifts between rates or modes (or both) of trait evolution are tightly constrained to the Late Miocene (11–5 Ma). Red-to-blue coloured line shows a global trend in palaeotemperature through the Cenozoic, data from Zachos et al. [3]. (b) Trends in the dispersal history of Australian radiations from the Early Miocene to present, as inferred from BioGeoBears analyses of empirical and simulated data (i.e. species distributions are observed as biome occurrences). The observed trend in the proportion of allopatric dispersal events (in green) exceeds the expected simulated proportion (purple), in the Late Miocene, coinciding with constraints on body size evolution of select Australian vertebrate clades. Jagged and Loess-smoothed dispersal curves represent two visualization methods of the same trend. Grey dots show palaeotemperature data and the red-to-blue line shows a best fit trend in palaeotemperature data. Note: scales of temperature and time differ between (a) and (b). MMCO, Mid-Miocene climatic optimum.

Figure 2.

Comparative fit of models to body size data of Australian vertebrate clades finds a preference for rate-declining models (BMOU, BMOUi, EB, ENV). Models are categorized below the plot. BMOU, BMOUi and ENV models are not methodologically explicit rate-declining, but instead, empirical parameter estimates (electronic supplementary material, figures S3,S4,S6) inform this trend. The y-axis indicates the relative support for each model as Akaike weights (averaged across 100 posterior trees). The top models which account for a combined more than 0.75 of the AICc weight for each clade are noted on each stacked bar graph.

Figure 3.

Sympatric and allopatric species pairs display differing trends in body size evolution. Left and centre columns show trends in allopatry and sympatry as inferred using extant species occurrence data and reconstructed ancestral ranges from rase [51]. Left column: allopatric species pairs (orange lines) exhibit less phenotypic disparity than sympatric relatives (blue lines) and show more pronounced declines in trait disparity through the Miocene. Centre column: the proportion of divergence events which are allopatric (orange fill) increase through the Miocene in most radiations. These estimates differ slightly from those presented in the electronic supplementary material, figure S1 because of the data used (spatial occurrence records versus biome codings), but see the electronic supplementary material, figure S1 for comparison of trends across all clades using both geographical data. Right column: multi-rate Brownian Motion separate model estimates identify greater evolutionary rates (sigma) for sympatric (blue) sister taxa than allopatric (orange).