Functional Diversity of Evolutionary Novelties: Insights from Waterfall-Climbing Kinematics and Performance of Juvenile Gobiid Fishes

Abstract

Synopsis The evolution of novel functional traits can contribute substantially to the diversification of lineages. Older functional traits might show greater variation than more recently evolved novelties, due to the accrual of evolutionary changes through time. However, functional complexity and many-to-one mapping of structure to function could complicate such expectations. In this context, we compared kinematics and performance across juveniles from multiple species for two styles of waterfall-climbing that are novel to gobiid fishes: ancestral “powerburst” climbing, and more recently evolved “inching”, which has been confirmed only among species of a single genus that is nested within the clade of powerburst climbers. Similar net climbing speeds across inching species seem, at first, to indicate that this more recently evolved mode of climbing exhibits less functional diversity. However, these similar net speeds arise through different pathways: Sicyopterus stimpsoni from Hawai’i move more slowly than S. lagocephalus from La Réunion, but may also spend more time moving. The production of similar performance between multiple functional pathways reflects a situation that resembles the phenomenon of many-to-one mapping of structure to function. Such similarity has the potential to mask appropriate interpretations of relative functional diversity between lineages, unless the mechanisms underlying performance are explored. More specifically, similarity in net performance between “powerburst” and “inching” styles indicates that selection on climbing performance was likely a limited factor in promoting the evolution of inching as a new mode of climbing. In this context, other processes (e.g., exaptation) might be implicated in the origin of this functional novelty.

Bendy to the bone: Links between vertebral morphology and waterfall climbing in amphidromous gobioid fishes

“…This result partially supports our prediction that powerburst climbers may be more flexible at mid body than inching climbers. During climbing, power burst climbers rely on lateral undulations that require more mid‐body flexibility than inching climbers which move rectilinearly up the waterfalls (Blob et al, 2019; Schoenfuss & Blob, 2003). Additionally, in non‐climbing species ( E .…”

“…Among waterfall climbing gobies, two distinct forms of climbing have been identified (Schoenfuss & Blob, 2003). The ancestral and more widespread powerburst climbing mode uses lateral undulations to move vertically up waterfalls between periods of substrate attachment (Figure 1; Blob et al, 2019). The other form of climbing, inching, is restricted to the genus Sicyopterus and entails individuals climbing rectilinearly up waterfalls by alternating attachment of the pelvic disc and a second sucker formed from the mouth (Cullen et al, 2013).…”

Evolutionary optimization of an anatomical suction cup: Lip collagen content and its correlation with flow and substrate in Neotropical suckermouth catfishes (Loricarioidei)

“…Due to their flexible, highly depressed bodies, hillstream loaches (Balitoridae) are able to use their entire body as a sucker (De Meyer & Geerinckx, 2014). Clingfishes (Gobiosocidae), lumpsuckers (Cyclopteridae), and gobies (Gobiidae) have independently derived pelvic‐fin modifications that allow them to act as a suction cup (Blob et al, 2019; Blob, Rai, Julius, & Schoenfuss, 2006; Davenport & Thorsteinsson, 1990; Ditsche, Wainwright, & Summers, 2014; Maie, Schoenfuss, & Blob, 2012; Schoenfuss & Blob, 2003; Wainwright, Kleinteich, Kleinteich, Gorb, & Summers, 2013), whereas remoras have a highly modified spiny dorsal fin that serves the same function (Beckert, Flammang, & Nadler, 2015; Fulcher & Motta, 2006; Nadler et al, 2013). Cypriniform algae‐eaters (Gyrinocheilidae), some gobies, and suckermouth catfishes in both Africa (Mochokidae) and South America (Astroblepidae, Loricariidae) have mouths that are modified to act as oral suckers, allowing them to adhere to surfaces, often while simultaneously feeding and respiring (De Meyer & Geerinckx, 2014; Geerinckx, Brunain, Herrel, Aerts, & Adriaens, 2007; Gerstner, 2007; Macdonnell, 1990; MacDonnell & Blake, 1990; Maie et al, 2012; Schoenfuss & Blob, 2003).…”

Sticking to it: testing passive pull-off forces in waterfall-climbing fishes across challenging substrates

“…The mechanism type and its performance are highly dependent on the external conditions to which it is exposed to during adhesion Ditsche et al, 2017;England et al, 2016;Huber et al, 2007;Peng et al, 2014;Persson and Gorb, 2003;Stark et al, 2015). Moreover, the evolution of novel functional capacities such as adhesion can facilitate the ability of species to occupy new or expanded niches (Blob et al, 2019;Lister, 1976;Maie et al, 2012;Price et al, 2010).…”

“…A well-established example of attachment mechanisms in an evolutionary radiation can be found among amphidromous gobiid fishes (Blob et al, 2019;Schoenfuss and Blob, 2007). In species that exhibit this life cycle, adults breed in freshwater streams, but fry are swept downstream to the ocean upon hatching, where they develop for several months before returning as juveniles to adult habitats (Schoenfuss and Blob, 2003).…”