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

Abstract

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.

Fig. 1

Phylogenetic relationships of gobiid species from which climbing performance has been evaluated, based on previous published analyses (Taillebois et al. 2014). Geographic location of each taxon is indicated in parentheses after its name: HI, Hawai’i; RÉU, La Réunion; CARIB, Caribbean (Dominica). Modes of climbing are indicated to the right of species names. Stenogobius hawaiiensis is included for reference as a non-climbing outgroup taxon. Dashed line indicates differing phylogenetic relationships of the genus Awaous. Based on available data, inching evolved once within the genus Sicyopterus.

Fig. 2

Still image of juvenile S. lagocephalus, extracted from high-speed video footage, illustrating the anatomical landmarks that were digitized for kinematic analyses. Because the fish is filmed in ventral view through Plexiglas, references will be made to anatomical left and right, which are opposite of what they appear in the image. (1) anterior midline edge of upper lip; (2) right edge of lip; (3) left edge of lip; (4) posterior midline of oral sucker (for S. lagocephalus) or head (for C. acutipinnis); (5) base of right pectoral fin; (6) tip of right pectoral fin; (7) base of the left pectoral fin; (8) tip of the left pectoral fin; (9) anterior edge of pelvic sucker; (10–16) evenly spaced body axis points; (17) caudal peduncle.

Fig. 3

Comparative kinematics of juvenile waterfall-climbing gobies. (A) Inching climbers. Mean profiles for kinematic variables during inching climbing by S. stimpsoni from Hawai’i (n = 26 climbing cycles, left column; data from Schoenfuss and Blob 2003) and S. lagocephalus from La Réunion: (n = 86 climbing cycles, right column). All trials were normalized to the same time duration, and plots show mean ± SE for every 2% increment of locomotor cycle duration. (B) Powerburst climbers. Mean profiles for axial kinematics during vertical powerburst climbing by juvenile A. stamineus and L. concolor from Hawai’i (n = 17 climbing cycles, left column; data pooled for these species as reported by Schoenfuss and Blob 2003), S. punctatum from Dominica (n = 22 climbing cycles, middle column; data from Schoenfuss et al. 2011); and C. acutipinnis from La Réunion (n = 87 climbing cycles, right column). Top row: bars for each equal-length segment of the body plot the mean (± SE) maximum angle of that segment to the direction of travel at any point during the cycle. Bottom row: mean (± SE) maximum amplitudes throughout the climbing cycle for each of 11 equally spaced points along the length of the fish, normalized as a percentage of body length. Original data reported in Supplementary Table S1.

Fig. 4

Comparative climbing performance of juvenile waterfall-climbing gobies, measured over 20 cm distances. (A) Net speed including periods of rest, normalized for body size. (B) Speed during periods of movement only, normalized for body size. (C) Proportion of time spent moving during 20 cm trials. Boxes show 25th percentile, median, and 75th values; whiskers illustrate 10th and 90th percentile values; open circles indicate values outside these percentiles. Vertical dashed line in each plot divides species by climbing style (powerburst climbers on the left, inching climbers on the right). Colors represent differences in locality, with white boxes showing data from Hawaiian species derived from Blob et al. (2006), gray boxes data from Caribbean species derived from Schoenfuss et al. (2011), and orange boxes new data from Réunionese species. Different boldface letters above each box plot indicate significant differences between groups, determined by Kruskal–Wallis analyses with Dunn’s post-hoc tests, corrected for multiple comparisons (P < 0.05). As, A. stamineus; Lc, L. concolor; Sp, S. punctatum; Ca, C. acutipinnis; Ss, S. stimpsoni; Sl, S. lagocephalus. Original data and sample sizes are reported in Supplementary Table S2.