Evolutionary Novelty versus Exaptation

Abstract

Species exposed to extreme environments often exhibit distinctive traits that help meet the demands of such habitats. Such traits could evolve independently, but under intense selective pressures of extreme environments some existing structures or behaviors might be coopted to meet specialized demands, evolving via the process of exaptation. We evaluated the potential for exaptation to have operated in the evolution of novel behaviors of the waterfall-climbing gobiid fish genus Sicyopterus. These fish use an “inching” behavior to climb waterfalls, in which an oral sucker is cyclically protruded and attached to the climbing surface. They also exhibit a distinctive feeding behavior, in which the premaxilla is cyclically protruded to scrape diatoms from the substrate. Given the similarity of these patterns, we hypothesized that one might have been coopted from the other. To evaluate this, we filmed climbing and feeding inSicyopterus stimpsoni from Hawai’i, and measured oral kinematics for two comparisons. First, we compared feeding kinematics of S. stimpsoni with those for two suction feeding gobiids (Awaous guamensis and Lentipes concolor), assessing what novel jaw movements were required for algal grazing. Second, we quantified the similarity of oral kinematics between feeding and climbing in S. stimpsoni, evaluating the potential for either to represent an exaptation from the other. Premaxillary movements showed the greatest differences between scraping and suction feeding taxa. Between feeding and climbing, overall profiles of oral kinematics matched closely for most variables in S. stimpsoni, with only a few showing significant differences in maximum values. Although current data cannot resolve whether oral movements for climbing were coopted from feeding, or feeding movements coopted from climbing, similarities between feeding and climbing kinematics in S. stimpsoni are consistent with evidence of exaptation, with modifications, between these behaviors. Such comparisons can provide insight into the evolutionary mechanisms facilitating exploitation of extreme habitats.

Citation: Cullen JA, Maie T, Schoenfuss HL, Blob RW (2013) Evolutionary Novelty versus Exaptation: Oral Kinematics in Feeding versus Climbing in the Waterfall-Climbing Hawaiian Goby Sicyopterus stimpsoni. PLoS ONE 8(1): e53274. doi:10.1371/journal.pone.0053274

Editor: Hector Escriva, Laboratoire Arago, France

Received: September 27, 2012; Accepted: November 27, 2012; Published: January 4, 2013

Copyright: © 2013 Cullen et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This study was funded by the US National Science foundation (http://www.nsf.gov) IOS-0817911 (HLS) and IOS-0817794 (RWB), a St. Cloud State University Faculty Research Grant (HLS), and Clemson University Creative Inquiry Grant #479 (RWB, JAC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

* E-mail: rblob@clemson.edu