A total-evidence phylogenetic approach to understanding the evolution, depth transitions, and body-shape changes in the anglerfishes and allies (Acanthuriformes: Lophioidei)

Abstract

The anglerfishes and allies (Lophioidei) are a diverse group of fishes with over 400 carnivorous species that are renowned for their remarkable hunting behavior employing a modified first dorsal-fin spine to lure prey and adaptations such as "pseudo-walking," bioluminescence, and parasitic sexual dimorphism. Gaining a comprehensive understanding of their evolutionary history has been challenging, as previous studies using DNA sequence data or morphological traits have provided either inconsistent or contradictory results. We present a new comprehensive phylogenetic framework for the evolution of the Lophioidei, combining ultraconserved elements (UCEs), mitochondrial DNA sequence data, and morphological characters. Our findings reveal a monophyletic Lophioidei, positioned as the sister group to the Tetraodontoidei within a broader acanthuriform radiation. Goosefishes (Lophioideo) emerge as the stem anglerfish lineage, forming a sister clade with frogfishes (Antennarioideo) + batfishes (Ogcocephaloideo) and coffinfishes (Chaunacoideo) + deep-sea anglerfishes (Ceratioideo). We expanded the Antennariidae to include all previous frogfish (antennarioid) families as subfamilies while proposing a new subfamily, Fowlerichthyinae, to produce a stable monophyletic taxonomy for the Antennarioideo. Further, we evaluated previously and newly proposed morphological characters to diagnose the Lophioidei and Lophioideo. Our investigations demonstrated that several traditional synapomorphies are no longer diagnostic for the Lophioidei. Based on our phylogeny, a geometric morphometric analysis revealed significant differences in body shape among lophioid infraorders, especially in frogfishes and deep-sea anglerfishes, indicating the importance of habitat transitions on body-shape evolution. This study, integrating genome-scale nuclear, mitochondrial, and morphological data, provides a total-evidence perspective on the evolutionary history of lophioids and sheds light on their specializations and body-shape changes as they transitioned across and within environments.

Fig 1. Images of representative anglerfishes (Lophioidei).

Background colors associated with lophioid infraorders. Lophioideo: (A) Lophiomus setigerus, 160 mm SL, FMNH 121120 (dorsal and lateral view; anterior to left). Antennarioideo: (B) Histrio histrio, 138 mm SL, LACM 8975-1 (lateral view; anterior to left). (C) Antennatus strigatus, 81 mm SL, LACM 20677 (lateral view; anterior to left). Ogcocephaloideo: (D) Zalieutes elater, 75 mm SL, FMNH 89523 (dorsal and lateral view; anterior to left). (E) Dibranchus atlanticus, 137 mm SL, FMNH 65256 (dorsal and lateral view; anterior to left). Chaunacoideo: (F) Chaunax sp., 158 mm SL, LACM 44750-3 (lateral view; anterior to left). Ceratioideo: (G) Caulophryne polynema, 131 mm SL, LACM 33923-1 (lateral view; anterior to left). (H) Himantolophus sagamius, 348 mm SL, LACM 60082-1 (lateral view; anterior to left). (I) Cryptopsaras couseii, 175 mm SL, LACM 11231-1 (lateral view; anterior to left). (J) Linophryne densiramus, 60 mm SL, LACM 38440-1 (lateral view; anterior to left).

Fig 2. Prior phylogenetic hypotheses of inter and intraordinal relationships of anglerfishes (Lophioidei).

Phylogenetic hypotheses and data type highlighting intraordinal relationships from studies that include two or more lophioid taxa, at least one tetraodontoid taxon, and four of the six other common lophioid allies (Antigoniidae, Caproidae, Cepolidae, Priacanthidae, Scatophagidae, and Siganidae) in their analyses: (A) mitochondrial and nuclear DNA sequence data, (B) mitochondrial and nuclear DNA sequence data, (C) nuclear DNA sequence data, (D) mitochondrial and nuclear DNA sequence data, (E) mitochondrial and nuclear DNA sequence data, (F) mitochondrial and nuclear DNA sequence data with morphology, (G) mitochondrial and nuclear DNA sequence and (H) ultraconserved element DNA sequence data. Phylogenetic hypotheses and data type highlighting infraordinal relationships from studies that include 20 or more genera in their analysis: (I) morphology, (J) morphology, (K) mitochondrial genomes, (L) mitochondrial and nuclear DNA sequence data with morphology, (M) exonic, mitochondrial, and nuclear DNA sequence data, (N) mitochondrial and nuclear DNA sequence data, (O) ultraconserved element DNA sequence data and (P) ultraconserved element DNA sequence data. Asterisks (***) in panel O indicate swapped taxa (see discussion: Ceratioideo).

Fig 3. Geometric morphometric landmark positions.

(A) Position of fixed homologous landmark (black) and sliding semi-landmark (gray) locations used in this study. (B) Consensus anglerfish and allies body shape from geometric morphometric analysis.

Fig 4. UCE maximum-likelihood tree.

Colored circles on nodes indicate bootstrap values as follows: white 50% to 69%, gray 70% to 89%, black 90% to 100% based on 1,000 ultrafast bootstrap replicates. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 5. Molecular maximum-ikelihood tree.

Colored circles on nodes indicate bootstrap values as follows: white 50% to 69%, gray 70% to 89%, black 90% to 100% based on 1,000 ultrafast bootstrap replicates. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 6. Total-evidence maximum-likelihood tree.

Colored circles on nodes indicate bootstrap values as follows: white 50% to 69%, gray 70% to 89%, black 90% to 100% based on 1,000 ultrafast bootstrap replicates. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 7. Morphological character optimization on the total-evidence phylogeny of the Lophioidei, Tetraodontoidei, and outgroups.

Total-evidence phylogenetic analysis topology of Lophioidei and outgroups. Morphological characters optimized onto each node are represented by a circle with the corresponding character number listed above and the corresponding character state listed below. Circles with black fill-in are unique and unreversed characters. Circles with white fill-in are inferred to have transformed multiple times on the phylogeny.

Fig 8. Anglerfishes and allies habitat transitions.

Parsimony character-state analysis of habitat transitions of anglerfishes based on the total-evidence maximum-likelihood phylogeny. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 9. Anglerfishes and allies depth transitions.

Parsimony character-state analysis of benthic/demersal or pelagic preferences of anglerfishes based on total-evidence maximum-likelihood phylogeny. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 10. Relative warp analysis of anglerfish body shape depicting PC1 + PC2.

(A) Relative warp analysis consisting of 11 homologous landmarks and 19 sliding landmarks. Circle positions represent the average location in the morphospace for each genus. See S8 Table for genus-level labels. (B) Relative warp analysis organized by depth range. The color scheme for infraorders and families corresponds to Figs 1 and 2. Fish illustrations by Alex Maile.

Fig 11. Phylomorphospace visualization.

Phylomorphospace plot of principal components 1 and 2 incorporating the total-evidence phylogeny of the Lophioidei. Circle positions represent the average location in the morphospace for each genus. See S8 Table for genus-level labels. The color scheme for infraorders and families corresponds to Figs 1 and 2.

Fig 12. Elongated and non-elongated fin elements in lophioid larvae.

Illustrations highlighting the derived and ancestral states of dorsal- and pelvic-fin rays among lophioid infraorders: (A) Lophiodes (Lophioideo), elongated fin elements present; (B) Histrio (Antennarioideo), elongated fin elements absent. Fish illustrations by Alex Maile.