Phylogenetic relationships and the evolution of BMP4 in triggerfishes and filefishes (Balistoidea)

Abstract

The triggerfishes (family Balistidae) and filefishes (family Monacanthidae) comprise a charismatic superfamily (Balistoidea) within the diverse order Tetraodontiformes. This group of largely marine fishes occupies an impressive ecological range across the world's oceans, and is well known for its locomotor and feeding diversity, unusual body shapes, small genome size, and ecological and economic importance. In order to investigate the evolutionary history of these important fish families, we used multiple phylogenetic methods to analyze molecular data from 86 species spanning the extant biodiversity of Balistidae and Monacanthidae. In addition to three gene regions that have been used extensively in phylogenetic analyses, we include sequence data for two mitochondrial regions, two nuclear markers, and the growth factor gene bmp4, which is involved with cranial development. Phylogenetic analyses strongly support the monophyly of the superfamily Balistoidea, the sister-family relationship of Balistidae and Monacanthidae, as well as three triggerfish and four filefish clades that are well resolved. A new classification for the Balistidae is proposed based on phylogenetic groups. Bayesian topology, as well as the timing of major cladogenesis events, is largely congruent with previous hypotheses of balistid phylogeny. However, we present a novel topology for major clades in the filefish family that illustrate the genera Aluterus and Stephanolepis are more closely related than previously posited. Molecular rates suggest a Miocene and Oligocene origin for the families Balistidae and Monacanthidae, respectively, and significant divergence of species in both families within the past 5 million years. A second key finding of this study is that, relative to the other protein-coding gene regions in our DNA supermatrix, bmp4 shows a rapid accumulation of both synonymous and non-synonymous substitutions, especially within the family Monacanthidae. Overall substitution patterns in bmp4 support the hypothesis of stabilizing selection during the evolutionary history of regulatory genes, with a small number of isolated examples of accelerated non-synonymous changes detected in our phylogeny.

Evolutionary patterns of shape and functional diversification in the skull and jaw musculature of triggerfishes (Teleostei: Balistidae)

“…, Supporting Information). While gradual morphological transformation is certainly the broad pattern of cranial shape evolution in Balistidae, we find instances of both prominent shape diversification among triggerfishes that our previous phylogenetic analyses (McCord and Westneat, ) have shown to be closely related, and also significant convergence onto similar regions of morphospace by patristically disparate taxa. In our analyses, cranial shape convergence often appears to be the result of a rapid separation of closely related species in opposite directions in cranial shape space toward the region in phylomorphospace that is occupied by distantly related triggerfishes with the same dietary habit (Fig.…”

“…At least two, and often several, adult specimens from each of the triggerfish genera were examined (Table ) except in the case of the rare genus, Xenobalistes , for which a specimen was not available for dissection. The triggerfish taxonomic names utilized here follow those outlined in McCord and Westneat ().…”

“…This study used a recent reconstruction of the phylogenetic relationships of balistoid fishes as a framework for the phylogenetic analyses of cranial shape and jaw biomechanics presented here (McCord and Westneat, ). A topology of relationships for triggerfishes was extracted from this larger study based on three nuclear markers ( bmp4 , rag2 , and tmo4c4 ) and two mitochondrial regions ( 12S and 16S ) plus all available sequences for cytB , rag1 , COI and rhodopsin from GenBank, with the matrix containing 27 triggerfish species.…”

“…The Balistidae are a morphologically conspicuous group of temperate and tropical marine fishes (Kuiter and Debelius, ), with well‐resolved phylogenetic relationships (Santini et al, ; McCord and Westneat, ). The 42 triggerfish species in this family are typically solitary diurnal predators, and exhibit an exceptional range of ecological diversity (Carpenter and Niem, ).…”

Mosaicism in a newEocene pufferfish highlights rapid morphological innovation near the origin of crown tetraodontiforms

“…), tetraodontids (Santini et al . ) and monacanthids (McCord & Westneat ). One possible explanation for our divergence date estimates being more ancient than anticipated, and with greater uncertainty, is that both Arcila et al .…”