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Evolutionary History of Anglerfishes (Teleostei: Lophiiformes): A Mitogenomic Perspective

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Evolutionary History of Anglerfishes (Teleostei: Lophiiformes): A Mitogenomic Perspective

Masaki Miya et al. BMC Evol Biol.

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.

Figures

Figure 1
Figure 1
Representatives of the lophiiform suborders Lophioidei (A), Antennarioidei (B, C), Chaunacoidei (D), and Ogcocephaloidei (E). (A) Lophiodes reticulatus Caruso and Suttkus, 157 mm SL, UF 158902, dorsal and lateral views (photo by J. H. Caruso); (B) Antennarius commerson (Latreille), 111 mm SL, UW 20983 (photo by D. B. Grobecker); (C) Sympterichthys politus (Richardson), specimen not retained (photo by R. Kuiter); (D) Chaunax suttkusi Caruso, 107 mm SL, TU 198058 (photo by J. H. Caruso); (E) Halieutichthys aculeatus (Mitchill), 80 mm SL, specimen not retained, dorsal view (photo by J. H. Caruso). Courtesy of the American Society of Ichthyologists and Herpetologists.
Figure 2
Figure 2
Representatives of ceratioid families as recognized in this study-1. (A) Centrophrynidae: Centrophryne spinulosa Regan and Trewavas, 136 mm SL, LACM 30379-1; (B) Ceratiidae: Cryptopsaras couesii Gill, 34.5 mm SL, BMNH 2006.10.19.1 (photo by E. A. Widder); (C) Himantolophidae: Himantolophus appelii (Clarke), 124 mm SL, CSIRO H.5652-01; (D) Diceratiidae: Diceratias trilobus Balushkin and Fedorov, 86 mm SL, AMS I.31144-004; (E) Diceratiidae: Bufoceratias wedli (Pietschmann), 96 mm SL, CSIRO H.2285-02; (F) Diceratiidae: Bufoceratias shaoi Pietsch, Ho, and Chen, 101 mm SL, ASIZP 61796 (photo by H.-C. Ho); (G) Melanocetidae: Melanocetus eustales Pietsch and Van Duzer, 93 mm SL, SIO 55-229; (H) Thaumatichthyidae: Lasiognathus amphirhamphus Pietsch, 157 mm SL, BMNH 2003.11.16.12; (I) Thaumatichthyidae: Thaumatichthys binghami Parr, 83 mm SL, UW 47537 (photo by C. Kenaley); (J) Oneirodidae: Chaenophryne quasiramifera Pietsch, 157 mm SL, SIO 72-180. Courtesy of the American Society of Ichthyologists and Herpetologists.
Figure 3
Figure 3
Representatives of ceratioid families as recognized in this study-2. (A) Oneirodidae: Oneirodes sp., 31 mm SL, MCZ 57783 (photo by C. P. Kenaley); (B) Oneirodidae: Spiniphryne duhameli Pietsch and Baldwin, 117 mm SL, SIO 60-239; (C) Caulophrynidae: Caulophryne pelagica (Brauer), 183 mm SL, BMNH 2000.1.14.106 (photo by D. Shale); (D) Neoceratiidae: Neoceratias spinifer Pappenheim, 52 mm SL, with 15.5-mm SL parasitic male, ZMUC P921726 (after Bertelsen, 1951); (E) Gigantactinidae: Gigantactis gargantua Bertelsen, Pietsch, and Lavenberg, 166 mm SL, LACM 9748-028; (F) Linophrynidae: Photocorynus spiniceps Regan, 46-mm SL, with 6.2-mm SL parasitic male, SIO 70-326; (G) Linophrynidae: Haplophryne mollis (Brauer), 36 mm SL, MNHN 2004-0811; (H) Linophrynidae: Linophryne macrodon Regan, 28 mm SL, UW 47538 (photo by C. P. Kenaley); (I) Linophrynidae: Linophryne polypogon Regan, 33 mm SL, BMNH 2004.9.12.167 (photo by P. David). Courtesy of the American Society of Ichthyologists and Herpetologists.
Figure 4
Figure 4
Previously proposed phylogenetic hypotheses within the Lophiiformes. Inter-subordinal relationships based on (A) morphology [3] and (B) the mitochondrial 16 rDNA sequences [29]. Intra-subordinal relationships based on (C) morphologies for the Lophioidei [30], (D) Antennarioidei [3], (E) Ogcocephaloidei [31] and (F, G) Ceratioidei [32,33].
Figure 5
Figure 5
The best-scoring maximum likelihood (ML) tree derived from 12n3rRTn dataset. Numerals beside internal branches indicate bootstrap probabilities ≥50% based on 500 replicates. Scale indicates expected number of substitutions per site. Extremely long branch from Tetrabrachium ocellatum is shortened to one third of the original length.
Figure 6
Figure 6
A strict consensus of the three best-scoring maximum likelihood (ML) trees. The strict consensus trees are derived from the three datasets that treat third codon positions differently (12n3rRTn, 123nRTn, 12nRTn). Lasiognathus sp. was considered as a member of the Oneirodidae because it is deeply nested within the family and monophyly of the traditional Thaumatichthyidae (Thaumatichthys and Lasiognathus) is confidently rejected by AU test (diff -ln L = 500.1; P > 0.0000).
Figure 7
Figure 7
A strict consensus of the 11 most parsimonious tree derived from maximum parsimony (MP) analysis of 53 morphological characters. These morphological characters are applicable to the metamorphosed females only (71 characters used in Pietsch and Orr [33] minus 18 characters that are supposedly show reductive or simplified states; for details see text). The 11 MP trees had a total length of 100, a consistency index of 0.610, and a retention index of 0.835.
Figure 8
Figure 8
Maximum likelihood reconstruction of the male sexual parasitism in ceratioid anglerfishes. Four discrete character states were assigned to each terminal and ancestral character states were reconstructed on the ML tree (Figure 5) under an ML optimality criterion using Mesquite ver. 2.6 [56].
Figure 9
Figure 9
Divergence times of ray-finned fishes. Divergence times were estimated from the partitioned Bayesian analysis using a multidistribute program package [63]. A total of 25 nodes (A-Y) were used for time constraints (for details, see Table 4). Horizontal bars indicate 95% credible intervals of the divergence time estimation.
Figure 10
Figure 10
Divergence times of the 39 species of the Lophiiformes. Divergence times were estimated from the partitioned Bayesian analysis using a multidistribute program package [63]. A total of nine nodes (filled circles) were used for fixed time constraints.

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References

    1. Pietsch TW. In: Ontogeny and systematics of fishes. Moser HG, Richards WJ, Cohen DE, Fahay MP, Kendall MPJ, Richardson SL, editor. Lawrence, Kansas: American Society of Ichthyologists and Herpetologists; 1984. Lophiiformes: development and relationships; pp. 320–325. vol. Special Publication 1.
    1. Pietsch TW. Oceanic anglerfishes: extraordinary diversity in the deep sea. Berkeley, California: University of California Press; 2009.
    1. Pietsch TW, Grobecker DB. Frogfishes of the world: systematics, zoogeography, and behavioral ecology. Stanford, California: Stanford University Press; 1987. - PubMed
    1. Pietsch TW. Dimorphism, parasitism, and sex revisited: modes of reproduction among deep-sea ceratioid anglerfishes (Teleostei: Lophiiformes) Ichthyological Research. 2005;52:207–236. doi: 10.1007/s10228-005-0286-2. - DOI
    1. Gregory WK. Fish skulls: A study of the evolution of natural mechanisms. Transactions of American Philosophical Society. 1933;23:75–481.

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