Testing the adaptive radiation hypothesis for the lemurs of Madagascar

Abstract

Lemurs, the diverse, endemic primates of Madagascar, are thought to represent a classic example of adaptive radiation. Based on the most complete phylogeny of living and extinct lemurs yet assembled, I tested predictions of adaptive radiation theory by estimating rates of speciation, extinction and adaptive phenotypic evolution. As predicted, lemur speciation rate exceeded that of their sister clade by nearly twofold, indicating the diversification dynamics of lemurs and mainland relatives may have been decoupled. Lemur diversification rates did not decline over time, however, as predicted by adaptive radiation theory. Optimal body masses diverged among dietary and activity pattern niches as lineages diversified into unique multidimensional ecospace. Based on these results, lemurs only partially fulfil the predictions of adaptive radiation theory, with phenotypic evolution corresponding to an 'early burst' of adaptive differentiation. The results must be interpreted with caution, however, because over the long evolutionary history of lemurs (approx. 50 million years), the 'early burst' signal of adaptive radiation may have been eroded by extinction.

Keywords: diversification; ecological divergence; macroevolution.

Figure 1.

Example phylogeny and expected diversification rates (speciation–extinction) through time. Two clades differ in a trait or geography (circle versus star) that results in the star clade undergoing adaptive radiation. The star clade is predicted to have higher diversification rates (solid lines) than the circle clade (dashed line). The diversification rate of the star clade is predicted to slow towards the present related to niche-filling or other processes [7]. Alternatively, recent processes may have driven an increase in diversification rate of the star clade. The circle clade is predicted to have low and constant diversification over time.

Figure 2.

Rate-through-time plots. Graphs illustrate the mean instantaneous rate estimate for lemurs through time (black line), with 95% credible intervals (CIs) (grey shading). (a) The net diversification rate (speciation–extinction rate) increased towards the present and did not exhibit decreasing rates towards zero as expected if speciation was diversity-dependent and nearing equilibrium. (b) The rate of body mass evolution (σ² Brownian motion variance) exhibits the predicted early burst of high evolutionary rates early and decreasing rates towards the present consistent with the hypothesis that lemurs diversified in body mass most early after colonizing Madagascar and subsequent body mass evolution was low.

Figure 3.

The multidimensional ecospace. The niche breadth occupied by lemurs far exceeds that of lorisiforms (black points), but the occupied ecospace has contracted substantially because of the extinction of the giant lemurs. Variation among species in (natural log) body mass, diet and activity pattern were summarized into two axes using multidimensional scaling (MDS1 and 2, approximately 90% of variation). Each lemur family (coloured points, extinct in grey with crosses in legend) occupies distinct ecospace, within which lorisiforms fill only a small proportion. The giant extinct lemurs filled unique ecospace (dashed convex hull) beyond that of extant species (solid convex hull).