Evolutionary Novelty versus Exaptation: Oral Kinematics in Feeding versus Climbing in the Waterfall-Climbing Hawaiian Goby Sicyopterus stimpsoni

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 in Sicyopterus 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.

Does your lip stick? Evolutionary aspects of the mouth morphology of the Indo‐Pacific clinging goby of theSicyopterusgenus (Teleostei: Gobioidei: Sicydiinae) based on mitogenome phylogeny

“…The current data cannot resolve whether oral movements for climbing were co‐opted from feeding or feeding movements co‐opted from climbing. However, similarities between feeding and climbing kinematics in S. stimpsoni, for example, are consistent with evidence of exaptation with modifications, between these behaviors (Cullen, Maie, Schoenfuss, & Blob, ).…”

“…However, similarities between feeding and climbing kinematics in S. stimpsoni, for example, are consistent with evidence of exaptation with modifications, between these behaviors (Cullen, Maie, Schoenfuss, & Blob, 2013).…”

Multiple exaptations leading to fish sound production

“…Exaptation was introduced to make a distinction between the current utility of a trait and its historical origin (Larson, Stephens, Tehrani, & Layton, 2013). Few examples are found in the literature (Cullen, Maie, Schoenfuss, & Blob, 2013;Ostrom, 1979;Patek, Baio, Fisher, & Suarez, 2013), probably because of the prevalence of an adaptationist view of evolution within evolutionary biologists (Gould, 2002). The main argument depends on the fact that every structure is a modification of some previous form, suggesting that all modifications are adaptations.…”

Rapid adaptive evolution of scale-eating kinematics to a novel ecological niche

“…Determining how organisms use resources for the first time and occupy novel niches is an outstanding question in evolutionary ecology. Many changes accompany adaptation to a novel niche, and previous studies have investigated how shifts in behaviors (Bowman and Billeb, 1965;Tebbich et al, 2010;Curry and Anderson, 2012), morphologies (Ferry-Graham et al, 2001;Ferry-Graham, 2002;Hata et al, 2011;Davis et al, 2018), physiologies (Arias-Rodriguez et al, 2011;Tobler et al, 2015Tobler et al, , 2018 and kinematics (Janovetz, 2005;Patek et al, 2006;Cullen et al, 2013;McGee et al, 2013) can all facilitate this transition.…”