A new time-scale for ray-finned fish evolution

Abstract

The Actinopterygii (ray-finned fishes) is the largest and most diverse vertebrate group, but little is agreed about the timing of its early evolution. Estimates using mitochondrial genomic data suggest that the major actinopterygian clades are much older than divergence dates implied by fossils. Here, the timing of the evolutionary origins of these clades is reinvestigated using morphological, and nuclear and mitochondrial genetic data. Results indicate that existing fossil-based estimates of the age of the crown-group Neopterygii, including the teleosts, Lepisosteus (gar) and Amia (bowfin), are at least 40 Myr too young. We present new palaeontological evidence that the neopterygian crown radiation is a Palaeozoic event, and demonstrate that conflicts between molecular and morphological data for the age of the Neopterygii result, in part, from missing fossil data. Although our molecular data also provide an older age estimate for the teleost crown, this range extension remains unsupported by the fossil evidence. Nuclear data from all relevant clades are used to demonstrate that the actinopterygian whole-genome duplication event is teleost-specific. While the date estimate of this event overlaps the probable range of the teleost stem group, a correlation between the genome duplication and the large-scale pattern of actinopterygian phylogeny remains elusive.

Figure 1

Alternative trees and group names of the major living actinopterygian clades: polypterids (bichir and reedfish); chondrosteans (sturgeons and paddlefish); lepisosteids (garpike); amiids (bowfin); and teleosts. (a) Topology from morphological data, supporting the Neopterygii (Regan 1923; Patterson 1973). (b) ‘Ancient Fish Clade’ topology obtained from mitochondrial genomic data (Inoue et al. 2003; present analysis) and some nuclear genetic data (Venkatesh et al. 2001). α, the Actinopterygii; β, the Actinopteri; γ, the Neopterygii; δ, the ‘Ancient Fish Clade’.

Figure 2

Strict consensus of the 116 shortest trees from the parsimony analysis of the morphological dataset of fossil and Recent Actinopterygii. Bold lines indicate crown-group Neopterygii. (a) Discoserra pectinodon Lund (2000), from the Mississippian (Serpukhovian) of Montana, USA. Dermal skull of CM (Carnegie Museum) 35211B in lateral view, anterior to left. Standard neopterygian apomorphies include the presence of an interopercular bone (iop), a supraorbital (spo), the shape and separation of the maxilla (mx) from the preopercular (pop), and the presence of a coronoid process (cpr) on the lower jaw. (b) Discoserra pectinodon (CM 41009A): caudal fin, external view with scales showing row-reversal at the meeting of peduncle and flank squamation. Neopterygian apomorphies include an abbreviated heterocercal shape (cf. modern lepisosteids), widely separated fin rays and the posterior terminus of lateral-line canal (tlln) directed onto fin, rather than extending posterio-dorsally along vestigial caudal lobe of the main body axis. Further details of braincase, hyoid arch, axial and caudal endoskeleton are provided in the electronic supplementary material. (c) Brachydegma caelatum Dunkle (1939), a basal stem-group halecomorph from the Early Permian (Artkinsian) of Texas, USA. Skull and pectoral region of MCZ (Museum of Comparative Zoology, Harvard University) 6503 in lateral view, anterior to right. (d) Brachydegma caelatum, left antorbital, showing a fractured anterior process (antpr) and in-filled sensory canal. (e) Brachydegma caelatum, left maxilla in (upper) dorsal and (lower) lateral views. Apomorphies shared with Amia and its closest fossil relatives include large median gular (mgu), maxilla (mx) with indented rear margin and horizontal median shelf or process (mpr), and antorbital (ao) with tapering anterior process (antpr). Neopterygian apomorphies include the presence of supraorbital (spo), accessory postcleithrum (apcl) and coronoid process (cpr) on the lower jaw. antpr, anterior process; ao, antorbital; aplcl, accessory postcleithrum; cl, cleithrum; cpr, coronoid process; dpt, dermopterotic; dsp, dermosphenotic; fb, basal fulcra; frf, fringing fulcra; hp, hypurals; io, infraorbital; iop, interoperculum; la, lachrymal; lgu, lateral gular; lpt, lepidotrichia; mgu, median gular; mpr, mesial process; mx, maxilla; op, opercular; pmx, premaxilla; pop, preoperculum; qj, quadratojugal; qu, quadrate; ro, rostral; sbo, suborbital; scb?, possible scale-bone; scl, supracleithrum; smb, smooth unornamented band; sop, subopercular; spo, supraorbital; tlln, terminal lateral-line scale.

Figure 3

Phylogenetic relationships among actinopterygians inferred from partitioned Bayesian analysis of 2520 bp of concatenated nucleotide sequences of four nuclear genes (excluding third codon positions). All teleost concatenated sequences belong to either paralogue groups ‘a’ (green) or ‘b’ (blue), whereas amiid, lepisosteid and chondrostean sequences fall outside of the teleost paralogue groups, indicating that the actinopterygian whole-genome duplication is specific to teleosts. The numbers on internal branches are (from top to bottom): Bayesian posterior probabilities and maximum-likelihood bootstrap proportions from nucleotide sequences, and quartet puzzling support values from amino acid sequences.

Figure 4

A new time-scale for actinopterygian evolution. A schematic providing comparison between teleost and neopterygian divergence date estimates derived from current and previous studies. Above geological column: previous fossil estimates (blue; Gardiner 1993; Grande & Bemis 1998; Arratia 2000) and previous mitochondrial genomic estimates (black; 1 or 2 depending on the method applied, Inoue et al. 2005; Yamanoue et al. 2006). Note a large disparity between divergence dates from previous fossil and mitochondrial datasets. Below geological column: divergence date estimates from the current study derived from fossil (blue), mitochondrial genomic (black) and nuclear genetic (red) data. Note congruent date estimates for the neopterygian divergence, but disagreement for the teleost date persists among different datasets. Phylogeny of Recent and fossil actinopterygians (simplified topology from the reweighted analysis of results in figure 2) plotted with divergence dates, illustrating the impact of Discoserra (Lund 2000) and Brachydegma (Dunkle 1939). Bold lines indicate the crown-group Neopterygii. Branch tips mark the earliest taxon occurrences in the geological record (subsequent taxon ranges not shown). Grey arrows juxtapose fossil dates for key events in vertebrate evolution (dates are conservative palaeontological estimates derived from Janvier (1996), Smith & Sansom (2001) and Long (2001); justification of the osteichthyan crown node can be found in the electronic supplementary material), highlighting discrepancies with previous molecular estimates of the teleost evolutionary time-scale. Geological column dates in Myr ago from Gradstein et al. (2004); series name abbreviations: L, Lower; Ll, Llandovery; M, Middle; Mis, Mississippian; Pen, Pennsylvanian; U, Upper.