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.

Lizards, toepads, and the ghost of hurricanes past

“…First, they surveyed toepad size in 12 populations of Anolis sagrei, a widely distributed Caribbean species (2). After correcting for body size and phylogenetic nonindependence, they found that relative toepad size correlated positively with the number of hurricanes (zero to four) in the last 70 y, in line with their finding with A. scriptus.…”

“…The anoles on Water Cay and Pine Cay perch mainly on small branches in the lower 3 m of vegetation. Donihue et al (1,2) propose that larger toepads enhance clinging ability and that this is adaptive in a wind storm because individuals that lose their grip might become injured or killed when landing, or even blown out to sea. Fritillary butterflies on isolated, windy islands in the Baltic have evolved enhanced grip, perhaps for similar reasons (6).…”

“…These sets of studies (1, 2) demonstrate an association between toepad size and hurricanes and do so not only on a local, shortterm scale but also on a geographic, long-term scale. Moreover, they find that this association seems to persist over decades and across the phylogeny (2).…”

“…By returning to the islands 13 mo later and measuring lizards in exactly the same manner as before, Donihue et al (2) discovered that the next generation of lizards had enlarged toepads, just like the hurricane survivors (1). Despite the lack of genetic data, this is strong evidence of an abrupt evolutionary change caused by selection.…”

“…1). In PNAS, Donihue et al (2) now report a follow-up study and show that offspring of 2017 survivors also had large toepads, strongly suggesting a genetically based shift. Furthermore, they evaluated whether the toepad × hurricane pattern would hold for other species of Anolis in the Neotropics.…”