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Who, When, and How Much? The Context Dependency of Rapid Evolution in Response to a Dietary Shift

Abstract

A population of Italian Wall Lizards (Podarcis sicula) on a small island in Croatia has become primarily herbivorous and morphologically distinct from its source population on a nearby island in ~30 generations, making it a compelling example of rapid evolution. What changes in digestive physiology and morphology have facilitated this switch to a novel diet? How does this dietary shift affect digestive performance? Do these accommodations for plant eating vary through time or with aspects of the lizards’ life history? I compared gut size and histology, eight digestive enzyme activities, and products of microbial fermentation across the two island populations, with selected comparisons to a mainland outgroup of P. sicula. The newly omnivorous population had several targeted biochemical differences in their hindguts compared to their source population, but no large-scale changes in physiology or gut morphology to match the scale and direction of divergence in their diets. In fact, island-mainland effects were far more prominent, even between insectivorous populations.

To test digestive performance, in the lab I fed lizards insect, mixed, or plant diets daily (high frequency, island males only) or on alternating days (low frequency, island and mainland males and females). When fed with high frequency, the newly omnivorous population was better at digesting plant proteins than their source population counterparts. However, when feed a low frequency, the males did not differ by population on any diet type. The females from the insectivorous source population, however, digested insect diets less efficiently than the other two populations.

To better elucidate dietary differences between the new and source populations lizards, I used stable isotope analyses to track 13C and 15N enrichment in their livers in concert with measurements of body and gut size over time and in males and females. Isotopic enrichment and gut length vary considerably by both year and season and suggest that the diet these lizards actually digest is not as different between the populations as stomach contents have suggested. Measurements of six digestive enzymes show differing patterns between populations depending on season and sex. The lizards’ responses to this dietary shift are dependent on multiple contexts.

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