Explosive morphological diversification of spiny-finned teleost fishes in the aftermath of the end-Cretaceous extinction

Abstract

The spiny-finned teleost fishes (Acanthomorpha) include nearly one-third of all living vertebrate species and assume a bewildering array of bodyplans, but the macroevolutionary assembly of modern acanthomorph biodiversity remains largely unexplored. Here, I reconstruct the trajectory of morphological diversification in this major radiation from its first appearance in the Late Cretaceous to the Miocene using a geometric morphometric database comprising more than 600 extinct species known from complete body fossils. The anatomical diversity (disparity) of acanthomorphs is low throughout the Cretaceous, increases sharply and significantly in the wake of the Cretaceous-Palaeogene (K-P) extinction, and shows little change throughout subsequent Cenozoic intervals. This pattern of morphological diversification appears robust to two potential biasing factors: the 'Lagerstätten effect', and the non-random segregation of rare and common taxa along phenotypic axes. Dissecting the trajectory of acanthomorph radiation along phylogenetic lines reveals that the abrupt post-extinction increase in disparity is driven largely by the proliferation of trophically diverse modern groups within Percomorpha, a spiny-fin subclade containing more than 15 000 living species and identified as showing a substantially elevated diversification rate relative to background vertebrate levels. A major component of the Palaeogene acanthomorph radiation reflects colonization of morphospace previously occupied by non-acanthomorph victims of the K-P. However, other aspects of morphological diversification cannot be explained by this simple ecological release model, suggesting that multiple factors contributed to the prolific anatomical radiation of acanthomorphs.

Figure 1.

Acanthomorph morphometrics. (a) Landmark scheme. Fixed landmarks are indicated by circles filled in grey and marked by numerals, while semilandmarks are marked by circles filled in white. Grey-filled circles containing an asterisk indicate fixed landmarks that serve as anchor points for intervening semilandmarks. Fixed landmarks record (moving clockwise, starting with the snout): 1, anterior tip of upper jaw (premaxilla); 2, joint between braincase and vertebral column; 3, posterodorsal tip of braincase (supraoccipital crest); 4, anterior insertion of dorsal fin; 5, posterior insertion of dorsal fin; 6, insertion of first ray of dorsal lobe of caudal fin; 7, distal tip of first principal ray of caudal fin (dorsal lobe); 8, posterior margin of caudal fin between dorsal and ventral lobes; 9, distal tip of first principal ray of caudal fin (ventral lobe); 10, insertion of first ray of ventral lobe of caudal fin; 11, posterior insertion of anal fin; 12, anterior insertion of anal fin; 13, ventral tip of pectoral girdle; 14, lower jaw joint. (b) Mean species values plotted on RW1 and RW2, which together account for over 62 per cent of overall variance. Symbols marking species indicate geological interval (eLK, early Late Cretaceous; lLK, late Late Cretaceous; P–eE, Palaeocene–early Eocene; mE–lE, Middle–Late Eocene; O, Oligocene; M, Miocene). Deformation grids indicate shapes found at extreme values along each axis, and fossils correspond to taxa approximating these morphologies. Higher axes given in the electronic supplementary material.

Figure 2.

Patterns of diversification in acanthomorph teleosts. Abbreviations for stratigraphic intervals are those used in figure 1, with date estimates shown for the beginning and end of each bin. (a) Morphospace occupancy during acanthomorph history. White circles represent percomorphs, black circles indicate other acanthomorphs. (b) Acanthomorph disparity expressed as multivariate variance of significant RW axes (RW1–RW4). Error bars are ±1 s.d. generated from 10 000 bootstrap pseudoreplicates. Asterisk (*) marks a significant increase in disparity between the lLK and P–eE (LR = 8.390 × 10⁷; Student's t-test: t = 1.89, d.f. = 207, p = 0.0313). (c) Percomorph contribution to overall acanthomorph disparity (percomorph partial disparity/acanthomorph disparity). Error bars are ±1 s.d. generated from 10 000 bootstrap pseudoreplicates. (d) Percomorph contribution to overall acanthomorph richness surveyed in this analysis. Error bars are 95 per cent binomial confidence intervals.

Figure 3.

Major aspects of acanthomorph diversification in the early Cenozoic are consistent with the refilling of morphospace vacated by non-acanthomorph victims of the end-Cretaceous extinction. Ordinations differ from those in figures 1b and 2a in excluding landmarks 4, 5, 11 and 12 (see explanation in text). (a) Acanthomorphs from the P–eE. Acanthomorphs belonging to predatory clades hypothesized to represent ecological replacements of non-acanthomorph victims (Cavin 2001; Friedman 2009; electronic supplementary material) are indicated by white circles. Images are, from left to right and top to bottom, representatives of †Rhamphognathidae, Pomatomidae, †Palaeorhynchidae, Carangidae, †Blochiidae, Scombridae, Sphyraenidae. (b) All Cretaceous acanthomorphs (eLK and lLK) plus non-acanthomorph victims of the K–P falling outside the morphological envelope of survivors in Friedman (2009). White triangles represent extinction victims. Images are, from left to right and top to bottom, representatives of †Pachyrhizodontidae, †Saurocephalidae, †Cimolichthyidae, †Aspidorhynchidae and †Enchodontidae. See the electronic supplementary material for full listing of victims and putative replacements.