Overshooting dynamics in a model adaptive radiation

Abstract

The history of life is punctuated by repeated periods of unusually rapid evolutionary diversification called adaptive radiation. The dynamics of diversity during a radiation reflect an overshooting pattern with an initial phase of exponential-like increase followed by a slower decline. Much attention has been paid to the factors that drive the increase phase, but far less is known about the causes of the decline phase. Decreases in diversity are rarely associated with climatic changes or catastrophic events, suggesting that they may be an intrinsic consequence of diversification. We experimentally identify the factors responsible for losses in diversity during the later stages of the model adaptive radiation of the bacterium Pseudomonas fluorescens. Proximately, diversity declines because of the loss of biofilm-forming niche specialist morphotypes. We show that this loss occurs despite the presence of strong divergent selection late in the radiation and is associated with continued adaptation of resident niche specialists to both the biotic and abiotic environments. These results suggest that losses of diversity in the latter stages of an adaptive radiation may be a general consequence of diversification through competition and lends support to the idea that the conditions favouring the emergence of diversity are different from those that ensure its long-term maintenance.

Figure 1.

Dynamics of radiation. (a) Mean morphological richness; (b) total metabolic richness (diamonds and solid line; see text) and metabolic disparity (squares and dashed line; see text) over the course of the radiation. Error bars represent ±1 s.e.m.

Figure 2.

Dynamics of morphotype diversity in a full factorial transplant experiment. Filled circles represent early (2-day) communities, while open circles are late (8-day) communities. Each point is the average of three replicates. Error bars represent ±1 s.e.m.

Figure 3.

Frequency-dependent fitness functions between smooth and wrinkly spreader pairs isolated from early and late in the radiation. Each point represents the outcome of a single competition at different starting frequencies between smooth and wrinkly pairs isolated from early (filled circles) or late (open circles). The two estimates of frequency-dependent selection are statistically indistinguishable.

Figure 4.

Outcome of four-way competition experiments between clones isolated from 96 or 200 h against ancestral clones. Each bar represents the average relative fitness for a derived genotype relative to an ancestral genotype of the same ecomorph (n = 3, error bars represent 1 s.e.m.). Asterisks indicate which estimates are significantly greater than 0. (a) Wringly-spreader and (b) smooth.