UC Berkeley

Adaptive radiations are thought to be one of the most important processes generating biological diversity on Earth. Although the existence of adaptive radiations is not in doubt, the exact mechanisms via which adaptation to different habitats translates into lineage splitting has been debated for over a century. Since the time of Darwin, biologists have invoked trade-offs during adaptation to environmental gradients as being the key to linking adaptation to species formation. However, identification of the causal gradients, trade-offs and extrinsic selective regimes involved in adaptive or ecological speciation requires detailed fieldwork and experimentation and cannot be inferred using genetic or observational data alone.

This series of studies provides an empirical, experimental basis for the conclusion that adaptation to different habitats is driving divergence in Encelia (Asteraceae) a genus of perennial desert shrubs that has radiated extensively throughout the Mojave and Sonoran deserts. Encelia is an ideal system for studying the mechanisms of adaptation and speciation because all taxa are completely interfertile, and many are considered habitat specialists and form hybrid zones wherever their distributions abut. Reciprocal transplant field experiments between two taxa, Encelia palmeri and E. ventorum, showed that extremely strong postzygotic divergent natural selection is primarily responsible for preventing species fusion. A resource manipulation experiment between the same two species further showed that this was due to trade-offs caused by a gradient in water availability between dune and desert habitats. Patterns of seed germination, herbivory, and burial by sand were also important and showed interactions with taxa and habitat indicating that divergent selection at this site is complex and multifaceted.

A second study involving the same two species asked whether a signature of postzygotic selection can be seen in the distribution of phenotypes through time and along a gradient of habitat disturbance. I found that novel phenotypes suggestive of recombination are produced at a high frequency but are not present in the adult population indicating a role for postzygotic natural selection in removing the products of recombination from the population. This conclusion was further strengthened by looking at disturbed versus undisturbed habitats. Disturbed habitats contained novel phenotypes suggestive of recombination that were absent in the undisturbed sites indicating that the hybrid swarms that frequently follow disturbance are likely caused by an alteration of postzygotic selective pressures. The higher resource availability of the disturbed sites suggests that a relaxation of selection is likely responsible.

These results are elaborated on further by conducting a literature review of cases where hybridization, species fusion or hybrid swarm formation are associated with disturbances or changes in environmental forcing factors. I found that there are many cases in the literature that describe taxa maintained primarily if not solely by extrinsic postzygotic selection, although this appeared to be more true for plants than animals. Animals, in contrast, were isolated primarily by prezygotic barriers including allopatry and sexual selection. This discrepancy may help explain the disagreement between zoologists and botanists for the past century about species definitions; zoologists have typically favored prezygotic criteria while many botanists have pointed out that definitions based on reproductive compatibility fail to capture much of the variation observed among plants.

Finally, I conducted a common garden experiment and an analysis of climatic niches with eight species in Encelia in order to determine whether there is evidence that selection is driving divergence among other taxa in the genus in addition to E. palmeri and E. ventorum. All taxa studied showed strong climatic differentiation according to temperature and precipitation, and trait divergence in the group was high with some taxa showing evidence of the evolution of key traits allowing colonization of high altitude and hyper-saline habitats. Despite this, trait variation did not reliably follow the predictions of leaf economic theory either within or among taxa. This may be due to the existence of multiple alternative ecologically equivalent strategies that may introduce noise into low-dimensional analyses of functional traits and climate. There were, however, exceptions to this pattern. Specific leaf area showed coherent variation within taxa but not among taxa, and ecotypes E. farinosa also varied in the directions predicted by leaf economic theory for nearly all of the traits examined.

These and previous studies establish Encelia as a classic case of adaptive radiation and underscore the importance of empirical, field-based studies for disentangling the complex mechanisms driving adaptation and the formation of new species.