Hurricane effects on Neotropical lizards span geographic and phylogenetic scales

Abstract

Extreme climate events such as droughts, cold snaps, and hurricanes can be powerful agents of natural selection, producing acute selective pressures very different from the everyday pressures acting on organisms. However, it remains unknown whether these infrequent but severe disruptions are quickly erased by quotidian selective forces, or whether they have the potential to durably shape biodiversity patterns across regions and clades. Here, we show that hurricanes have enduring evolutionary impacts on the morphology of anoles, a diverse Neotropical lizard clade. We first demonstrate a transgenerational effect of extreme selection on toepad area for two populations struck by hurricanes in 2017. Given this short-term effect of hurricanes, we then asked whether populations and species that more frequently experienced hurricanes have larger toepads. Using 70 y of historical hurricane data, we demonstrate that, indeed, toepad area positively correlates with hurricane activity for both 12 island populations of Anolis sagrei and 188 Anolis species throughout the Neotropics. Extreme climate events are intensifying due to climate change and may represent overlooked drivers of biogeographic and large-scale biodiversity patterns.

Keywords: Anolis; cyclones; extreme climate events; rapid evolution.

Fig. 1.

Anolis scriptus, like other anoles, use specialized toepads to cling to surfaces (D, Inset images: A lizard clings to a perch while experiencing hurricane-force winds in a performance experiment; see ref. 3). Populations of A. scriptus on Pine and Water Cays in the TCI (C) that survived 2017’s Hurricanes Irma and Maria had relatively larger toepads on average than the populations surveyed before the storms (3). When we resurveyed the populations in 2019 (A and B) following the storms, those body size-corrected differences in toepad area persisted.

Fig. 2.

By measuring toepad areas of individuals from 12 populations of A. sagrei (A), we found that populations that experienced more hurricanes in the last 70 y (red) had larger toepads than those that were hit less often (blue). In the map, each point corresponds to an island population, the size of the point corresponds to the relative toepad surface area of that population, and the color to the number of hurricanes experienced in the last 70 y. Regressions are of phylogenetically and body size-corrected toepad area residuals for forelimbs (B) and hindlimbs (C). See SI Appendix for additional detail about the hurricane activity calculation.

Fig. 3.

Across the full geographic expanse of the Anolis clade, here with each point representing one of 188 species, toepad area—accounting for phylogeny and body size—is significantly positively correlated with the number of hurricanes experienced by that species over the last 70 y. (A) Each point represents the centroid of a species range, the color of that point indicates the mean number of hurricanes experienced across the species’ range, and the size of the point corresponds to the average body size-corrected toepad area. For clarity, we highlighted the species on the mainland and on each of the Greater Antillean islands in callouts and ordered them by increasing hurricane activity. Size-corrected residuals of insular forelimb (B) and hindlimb (C) toepad areas are positively related to hurricane activity.