Article

Evolutionary history of anglerfishes (Teleostei: Lophiiformes): a mitogenomic perspective

Natural History Museum and Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan.
BMC Evolutionary Biology (Impact Factor: 3.41). 02/2010; 10:58. DOI: 10.1186/1471-2148-10-58
Source: PubMed

ABSTRACT The teleost order Lophiiformes, commonly known as the anglerfishes, contains a diverse array of marine fishes, ranging from benthic shallow-water dwellers to highly modified deep-sea midwater species. They comprise 321 living species placed in 68 genera, 18 families and 5 suborders, but approximately half of the species diversity is occupied by deep-sea ceratioids distributed among 11 families. The evolutionary origins of such remarkable habitat and species diversity, however, remain elusive because of the lack of fresh material for a majority of the deep-sea ceratioids and incompleteness of the fossil record across all of the Lophiiformes. To obtain a comprehensive picture of the phylogeny and evolutionary history of the anglerfishes, we assembled whole mitochondrial genome (mitogenome) sequences from 39 lophiiforms (33 newly determined during this study) representing all five suborders and 17 of the 18 families. Sequences of 77 higher teleosts including the 39 lophiiform sequences were unambiguously aligned and subjected to phylogenetic analysis and divergence time estimation.
Partitioned maximum likelihood analysis confidently recovered monophyly for all of the higher taxa (including the order itself) with the exception of the Thaumatichthyidae (Lasiognathus was deeply nested within the Oneirodidae). The mitogenomic trees strongly support the most basal and an apical position of the Lophioidei and a clade comprising Chaunacoidei + Ceratioidei, respectively, although alternative phylogenetic positions of the remaining two suborders (Antennarioidei and Ogcocephaloidei) with respect to the above two lineages are statistically indistinguishable. While morphology-based intra-subordinal relationships for relatively shallow, benthic dwellers (Lophioidei, Antennarioidei, Ogcocephaloidei, Chaunacoidei) are either congruent with or statistically indistinguishable from the present mitogenomic tree, those of the principally deep-sea midwater dwellers (Ceratioidei) cannot be reconciled with the molecular phylogeny. A relaxed molecular-clock Bayesian analysis of the divergence times suggests that all of the subordinal diversifications have occurred during a relatively short time period between 100 and 130 Myr ago (early to mid Cretaceous).
The mitogenomic analyses revealed previously unappreciated phylogenetic relationships among the lophiiform suborders and ceratioid familes. Although the latter relationships cannot be reconciled with the earlier hypotheses based on morphology, we found that simple exclusion of the reductive or simplified characters can alleviate some of the conflict. The acquisition of novel features, such as male dwarfism, bioluminescent lures, and unique reproductive modes allowed the deep-sea ceratioids to diversify rapidly in a largely unexploited, food-poor bathypelagic zone (200-2000 m depth) relative to the other lophiiforms occurring in shallow coastal areas.

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    • "Molecular data have the potential to provide this support by offering a much larger pool of characters from which to draw, one that increases rapidly as additional loci are sampled. In many cases the trees resulting from analyses of these data represent hypotheses of species' relationships that are incongruent with previous morphological studies, with abundant examples coming from varied lineages of ray-finned fishes (e.g., Near et al., 2000; Moyer et al., 2004; Miya et al., 2010), as well as a broad range of lineages across the Tree of Life (e.g., Poe, 1996; Graham et al., 1998; Williams et al., 2003). Such disagreement between data sets is not limited to comparisons of morphological and molecular phylogenies. "
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    • "Lophioidei was recovered as the sister group to the rest of the anglerfish suborders. This result agrees with past molecular (Miya et al., 2010) and morphological (Pietsch and Grobecker, 1987) studies. "
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    • "Complete mitogenome sequences naturally contain the mitochondrial barcoding region, allowing data-internal verification of sample identification. In addition, complete mitogenome sequences can be used to design primers useful for population genetic or phylogenetic work (Sorenson et al., 1999), or to address questions in higher-level phylogeny (Gibson et al., 2005; Kumazawa, 2007; Miya et al., 2010; Slack et al., 2007; Zhang & Wake, 2009). The potential for mitochondrial applications of shotgun sequencing methods may depend on the tissue source of DNA, because tissues vary widely in their ratio of mitochondrial to nuclear DNA (Robin & Wong, 1988; Veltri et al., 1990). "
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