Molecular phylogenetics and evolutionary history of ariid catfishes revisited: a comprehensive sampling

Abstract

Background: Ariids or sea catfishes are one of the two otophysan fish families (out of about 67 families in four orders) that inhabit mainly marine and brackish waters (although some species occur strictly in fresh waters). The group includes over 150 species placed in approximately 29 genera and two subfamilies (Galeichthyinae and Ariinae). Despite their global distribution, ariids are largely restricted to the continental shelves due in part to their specialized reproductive behavior (i.e., oral incubation). Thus, among marine fishes, ariids offer an excellent opportunity for inferring historical biogeographic scenarios. Phylogenetic hypotheses available for ariids have focused on restricted geographic areas and comprehensive phylogenies are still missing. This study inferred phylogenetic hypotheses for 123 ariid species in 28 genera from different biogeographic provinces using both mitochondrial and nuclear sequences (up to approximately 4 kb).

Results: While the topologies obtained support the monophyly of basal groups, up to ten genera validated in previous morphological studies were incongruent with the molecular topologies. New World ariines were recovered as paraphyletic and Old World ariines were grouped into a well-supported clade that was further divided into subclades mainly restricted to major Gondwanan landmasses. A general area cladogram derived from the area cladograms of ariines and three other fish groups was largely congruent with the geological area cladogram of Gondwana. Nonetheless, molecular clock estimations provided variable results on the timing of ariine diversification (approximately 105-41 mya).

Conclusion: This study provides the most comprehensive phylogeny of sea catfishes to date and highlights the need for re-assessment of their classification. While from a topological standpoint the evolutionary history of ariines is mostly congruent with vicariance associated with the sequence of events during Gondwanan fragmentation, ambiguous divergence time estimations hinders assessing the vicariant hypothesis on a temporal framework. Further examination of ariid fossils might provide the basis for more accurate inferences on the timing of ariine diversification.

Figure 1

Approximate distribution of ariids. Some shaded areas represent extrapolated localities [after [19]].

Figure 2

Alternative hypotheses of relationships among ariid taxa. (A) Kailola's [15] phylogeny on 45 Old World and eight New World ariid species based on 57 morphological characters. Taxa examined during this study are in bold; asterisks (*) indicate clades that are congruent with the topologies recovered (see Figure 3). (B) Betancur-R. et al.'s [19] phylogeny on 46 New World and three Old World ariid species. The summarized phylogeny is derived from trees obtained from mitochondrial (2842 bp), nuclear (978 bp), and morphological (55 characters) datasets. Both studies deal with different taxon-sampling schemes, and both topologies are highly incongruent regarding the position of Galeichthys, Ketengus typus and Cryptarius truncatus.

Figure 3

BI phylogeny of 124 arioid species derived from the mitochondrial dataset (2866 bp). Fifty percent majority rule consensus on ~2.15 × 105 post-burn-in trees (mean lnL-52160). (A) cladogram; thicker branches indicate clades that are congruent with MP and ML (Garli and RAxML) analyses. Asterisks (*) designate clade support (see also Additional file 2); capital letters indicate nodes referred in text and Additional file 2 (symbols and letters always on left of nodes); vertical bars indicate subfamilial divisions and distribution of major ariine groups. Generic placement for New World and Old World ariines follows Betancur-R. et al. [19] and Marceniuk and Menezes [21], respectively. Colored taxa indicate non-monophyletic genera validated by Marceniuk and Menezes (yellow and red taxa correspond to Notarius and Sciades sensu [21], respectively). Two letter country codes follow ISO-3166. (B) phylogram (Ariidae only) elucidating the short internodes at the base of the Ariinae and the rate variation across lineages (taxon arrangement follows the same order in both figures). Gray dots indicate long branches in N. lentiginosus (left) and H. sagor (right).

Figure 4

A remarkable example of morphological convergence. The genus Hexanematichthys sensu Kailola [15] includes two species ('Sciades' sagor and S. mastersi) and is defined by the presence of a broad and depressed head, a short and broad supraoccipital process (SP) and a large butterfly-shaped nuchal plate (NP), among other features. While the neurocrania of S. sagor and S. mastersi are most similar in this sample, the molecular evidence suggests that they are more closely related to Arius nenga (India-SE Asia clade) and Cochlefelis dioctes (Australia-New Guinea clade), respectively (see Figure 3). Also, Templeton and SH tests reject monophyly of Hexanematichthys (see Table 2). (A), AUM 46280, 87 mm cranial length (CL); (B), AUM 50242, 131 mm CL; (C), AUM 47562, 117 mm CL; (D), AUM 47507, 170 mm CL.

Figure 5

Area cladograms. (A) Geological area cladogram of Gondwanan progression (summarized by [48] based on [55] and [56]). Ariine area cladograms based on MP (B) and ML (C) topologies estimated on the combined dataset (see details in Table 1, Additional file 2). (D) Sparks and Smith [48] general area cladogram derived from the area cladograms of cichlids, aplocheiloid killifishes, and rainbowfishes (for particular area cladograms see [[48]: Fig. four]). (E) General area cladogram derived from the component analysis of the four fish groups using either MP (strict consensus of three optimal trees, minimal value = 51) or ML (strict consensus of three optimal trees, minimal value = 32) topologies. Widespread Netuma and Plicofollis were handled under assumption 2 [76-78,81] by arbitrarily removing all but one area from their distributions (areas used: India-SE Asia for Netuma, Australia-New Guinea for Plicofollis [79,80]). Letters in parentheses refer to nodes in Figure 3 and Additional file 2.