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

Abstract

BackgroundThe 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.ResultsPartitioned 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).ConclusionsThe 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.

Resolution of ray-finned fish phylogeny and timing of diversification

“…2A) (333.0-285.8 Ma), following the Devonian Age of Fishes. This estimate agrees with analyses of whole mtDNA genomes (28) and the assessment of a WGD event occurring in teleosts (29). The credibility of teleosts diversifying in the Paleozoic was challenged by analyses of the rag1 nuclear gene that estimated teleosts diversified during the Late Triassic to Middle Jurassic (20).…”

“…JX190073-JX191369). the most recent common ancestor of living teleosts range from 310 to 350 Ma based on whole mtDNA genome sequences (28), ∼320 Ma based on comparisons of paralogous gene copies resulting from the teleost whole-genome duplication (WGD) event (29), and 173-260 Ma based on fossil-calibrated nuclear gene phylogenies (7,19,20). Although these studies estimated ages for the crown teleost clade that are older than the fossil record, molecular age estimates across ray-finned fish lineages include those that are older, as well as younger, than fossil-based estimates.…”

A Dwarf Male Reversal in Bone-Eating Worms

“…Where phylogenetic studies have been done on other animal groups, the occurrence of dwarfs is arguably derived, e.g., in echiuran annelids [19]. Often, dwarf males have appeared independently multiple times in a clade, as in anglerfish [20], barnacles [21,22], and, arguably, in xylotrophic bivalves Current Biology Vol 25 No 2 [23][24][25]. Orb-web spiders (Nephilidae) show marked SSD, females being much larger than males, with a complex history of increases and decreases in size for both sexes [26].…”

First in situ observations of the deep-sea squid Grimalditeuthis bonplandi reveal unique use of tentacles

“…Luring is one form of aggressive mimicry, and there are numerous proposed occurrences of this type of aggressive mimicry in deep-sea organisms. Examples include: the cookie-cutter shark Isistius brasiliensis [27]; anglerfish, viperfish and dragonfish that possess one or more bioluminescent lures [27][28][29]; the siphonophore Erenna sp. that attracts prey with luminescence and flicking of the modified side-branches of their tentacles (tentilla) [30]; and various squids with photophore-tipped arms or tentacles [2,28].…”