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.

Introduction

Animals that live in, or travel through, extreme environments can be exposed to severe functional demands. However, species that have successfully penetrated such habitats often exhibit novel traits that help them to accommodate such demands [1], [2]. Gobioid fishes found in the streams of many volcanic, oceanic islands provide prominent examples of this pattern. Streams of volcanic islands are subject to a range of catastrophic disturbances including lava flows, hurricanes, and flash floods [3]. The ability of many gobioid species to persist in habitats subject to such extremes is facilitated by a complex, amphidromous life cycle [4]–[6]. Adult fish mate and deposit eggs in streams, but upon hatching the larvae are swept into the ocean where they develop for several months before returning to freshwater [4], [7], [8], providing an oceanic population reservoir from which disturbed streams can be repopulated [3].

To penetrate upstream habitats, many goby species must scale substantial waterfalls that can exceed tens of meters in height [9]. Such climbing is facilitated by the presence of a ventral sucker, common to all gobies, formed from the fusion of the pelvic fins [10], [11]. However, species of one goby genus, Sicyopterus, also exhibit a distinctive oral sucker that develops after larvae undergo a cranial metamorphosis that coincides with the return to freshwater, during which the mouth shifts from a terminal orientation to a subterminal position over the course of 36–48 h [12], [13]. The oral sucker facilitates use of a novel mechanism for accessing upstream habitats above waterfalls [9], [11], [14], [15]. This form of locomotion has been termed “inching” and requires alternate attachment of oral and pelvic discs to the rocky substrate, providing a slow, but steady, method of climbing that, in the Hawaiian species S. stimpsoni, allows individual fish to scale waterfalls up to 100 m tall [9], [10]. Juveniles from goby taxa that lack an oral disc, including Sicydiine outgroups to Sicyopterus such as the genera Sicydium and Lentipes [16], exhibit a different climbing behavior described as “powerburst” climbing. In this pattern, the pectoral fins are adducted before rapid undulation of the body, with no oral involvement in adhesion [9], [17]. Thus, it appears most parsimonious that the oral disc and cranial kinematics used by climbing Sicyopterus are derived, rather than basal features. Although the structural basis for the use of the mouth as a locomotor organ is clear in this genus, how did its novel locomotor strategy evolve?

In addition to its distinctive use of the mouth for locomotion, oral function during feeding also appears distinctive in Sicyopterus compared to other stream gobies, as exemplified by Hawaiian S. stimpsoni. A larval feeding strategy of capturing zooplankton changes to a juvenile strategy that involves scraping benthic diatoms from rocks [4], [18], [19]. In a broad sense, this behavior, like inching during waterfall climbing, also involves motion of the mouth against a substrate. With the mouth being used in generally similar ways for these different post-metamorphic behaviors, it is possible that, rather than evolving independently, jaw kinematics in one of these behaviors may simply have been coopted and implemented in a new behavior.

Numerous instances have been proposed in which a structure that had been used for one specific function appears to have been coopted for another function [20], suggesting this possibility in the behavioral evolution of S. stimpsoni and other members of the genus Sicyopterus. Such instances of evolutionary coopting have been termed “exaptations”[20]. In a classic example from the evolution of birds that was described in the paper that coined this term [20], feathers may have served originally to provide insulation and only later, after changes in feather shape and forelimb morphology, been coopted to serve a role contributing to sustained flight [20]. More recently proposed examples of exaptation have extended beyond structural features to include behavioral and biomechanical traits [21]–[24]. For example, juvenile chukar partridges display a behavior termed “wing-assisted incline running,” in which they flap small, immature wings in order to climb inclines. The discovery that such behaviors generate substantial lift suggests the potential that the functional capacities of even appendages with suboptimal wing morphology might have been coopted during the eventual evolution of flight [21]. In another example of the coopting of a motor behavior from one function to another, trap-jaw ants typically use the rapid closing strikes of their mandibles for prey capture, but can also use them to propel themselves into the air by simply reorienting strikes to be directed against the ground [22]. In a closer parallel to the gobiid fish system, previous studies have shown herbivorous benthic scraping abilities [25], [26] as well as station-holding abilities [27] among species of catfishes; however it is unclear how closely patterns of movement compare in such cases.

Although the feeding behavior of S. stimpsoni has been recognized as novel among Hawaiian gobiids, specific kinematic differences in comparison to other gobiid species have not been quantified. Moreover, while both climbing and feeding have been examined to some extent in S. stimpsoni, kinematic comparisons of these two behaviors that could help assess the potential for exaptation in this genus have not been performed. In this study, we measured the oral kinematics of climbing and feeding by S. stimpsoni for two sets of comparisons. First, to assess novel patterns of jaw motion required for algal grazing, we compared the feeding kinematics of S. stimpsoni with those previously published for two outgroup, suction feeding Hawaiian gobiids, Awaous guamensis and Lentipes concolor [28]. Second, in order to evaluate the potential for either feeding or climbing kinematics to represent the coopting of patterns of motion in the other behavior, we compared oral kinematics for these behaviors in S. stimpsoni. If the kinematics of these two behaviors were significantly different, it would be less likely that the performance of one function involved simple exaptation of the other. In contrast, if kinematics of these behaviors were similar, movements in one function may simply have been coopted for a different role in the other.

Highlighting the difficulty in formally identifying a trait as an exaptation, Lauder [29] identified four criteria for which evidence should be provided: (1) current utility of the trait, (2) selection for that trait in its current environment, (3) previous utility of the trait in an ancestral taxon for a different role than the current one, and (4) natural selection for that trait in the ancestral environment. Our previous studies have shown the utility of oral function in both climbing [9], [11], [30] and feeding [19] in S. stimpsoni, as well as selection on climbing performance [31], [32]. Because no species of Sicyopterus is known to use oral movements for one behavior (climbing or feeding) but not the other, it is difficult to establish a phylogenetic context that would point to one behavior being more likely ancestral, and it may not be possible to definitively evaluate which behavior might represent an exaptation. However, independent of which behavior came first, our primary goal is to consider whether the evolutionary mechanism of exaptation may have operated in this system, given the context of knowledge about utility and selection for feeding and climbing. The first step in such an assessment is to evaluate whether oral movements for climbing and feeding should be considered as the same trait, based on the extent of their similarity.