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Open Access Highly Accessed Research article

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

Masaki Miya1*, Theodore W Pietsch2, James W Orr3, Rachel J Arnold2, Takashi P Satoh4, Andrew M Shedlock5, Hsuan-Ching Ho6, Mitsuomi Shimazaki7, Mamoru Yabe7 and Mutsumi Nishida8

Author Affiliations

1 Natural History Museum and Institute, Chiba, 955-2 Aoba-cho, Chuo-ku, Chiba 260-8682, Japan

2 School of Aquatic and Fishery Sciences, College of Ocean and Fishery Sciences, University of Washington, Campus Box 355020, Seattle, WA 98195-5020, USA

3 National Marine Fisheries Service, Alaska Fisheries Science Center, 7600 Sand Point Way NE, Seattle, WA 98115, USA

4 Collection Center, National Museum of Nature and Science, 3-23-1 Hyakunincho, Shinjuku-ku, Tokyo 169-0073, Japan

5 Department of Organismic and Evolutionary Biology, Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138, USA

6 Institute of Marine Biology, National Taiwan Ocean University, 2 Peining Road, Keelung 202, Taiwan

7 Laboratory of Marine Biodiversity, Graduate School of Fisheries Sciences, Hokkaido University, 3-1-1 Minato-cho, Hakodate, Hokkaido 041-8611, Japan

8 Ocean Research Institute, The University of Tokyo, 1-15-1 Minamidai, Nakano-ku, Tokyo 164-8689, Japan

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BMC Evolutionary Biology 2010, 10:58  doi:10.1186/1471-2148-10-58

Published: 23 February 2010

Abstract

Background

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.

Results

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).

Conclusions

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.