Synergistic innovations enabled the radiation of anglerfishes in the deep open ocean

Brownstein, Chase1 ; Zapfe, Katerina2 ; Lott, Spencer1 ; Ghezeleyagh, Ava1 ; Harrington, Richard C.3 ; Dornburg, Alex2 ; Near, Thomas1

Published Feb 06, 2024; Updated Jun 06, 2024 on Dryad. https://doi.org/10.5061/dryad.9cnp5hqrb

Abstract

Major ecological transitions are thought to fuel diversification, but whether they are contingent on the evolution of certain traits called key innovations is unclear. Key innovations are routinely invoked to explain how lineages rapidly exploit new ecological opportunities . However, investigations of key innovations often focus on single traits rather than considering trait combinations that collectively produce effects of interest . Here, we investigate the evolution of synergistic trait interactions in anglerfishes, which include one of the most species-rich vertebrate clades in the bathypelagic, or ‘midnight,’ zone of the deep sea: Ceratioidea. Ceratioids are the only vertebrates that possess sexual parasitism, wherein males temporarily attach or permanently fuse to females to mate. We show that the rapid transition of ancestrally benthic anglerfishes into pelagic habitats occurred during a period of major global warming 50-35 million years ago. This transition coincided with the origins of sexual parasitism, which is thought to increase the probability of successful reproduction once a mate is found in the midnight zone, Earth’s largest habitat. Our reconstruction of the evolutionary history of anglerfishes and the loss of immune genes support that permanently-fusing clades have convergently degenerated their adaptive immunity. We find that degenerate adaptive immune genes and sexual body size dimorphism, both variably present in anglerfishes outside the ceratioid radiation, likely promoted their transition into the bathypelagic zone. These results show how traits from separate physiological, morphological, and reproductive systems can interact synergistically to drive major transitions and subsequent diversification in novel environments.

README: Reproductive innovation enabled radiation in the deep sea during an ecological crisis

https://doi.org/10.5061/dryad.9cnp5hqrb

This repository contains all data from the article "Reproductive innovation enabled radiation in the deep sea during an ecological crisis"

Description of the data and file structure

Ancestral_States_Phytools.zip ## Contains all data necessary for the phytools ancestral state reconstructions Angler_Reproduction.csv #reproduction trait file Angler_Locomotion.csv #locomotion trait file Immune_data.csv #immunogenetics trait file Angler_Dimorphism.csv #dimorphism trait file

Anglerfish_script_R.R ### R code to replicate all analyses in the paper

Anomaly_Finder.zip ##Contains all code and data necessary for the anomaly zone analysis anomaly_finder.py #python script to find anomaly zones Anomaly_Finder_Output_ASTRAL.tree #output IQ_TREE_CONCAT_anomaly_finder.tree #input IQTREE file

Chaunacidae_test.zip ##Mitochondrial phylogeny and genetic dissimilarity tests for Chaunacidae Chaunax_test.fas #fasta file containing alignments IQ_TREE_Output ##folder containing IQ-TREE output files

IQ-Tree_and_Astral.zip ##IQTREE and ASTRAL output iq_tree_concatenated_final ## folder containing output for concatenated IQ-TREE analysis iqtree_final ##folder containing output for iqtree gene trees run partitioned_iqtree_final ## folder containing output for partitioned concatenated IQ-TREE analysis Astral ## folder containing input and output for ASTRAL-III multispecies coalescent tree concordance_factors ## folder containing output for IQ-TREE concordance factor analysis

Paralog-ILS-test ##TOAST paralogy input and output really_long_branch ##folder containing gene trees with abnormally long singleton branches but passed TOAST gene_trees_TOAST_fail_ILS_only ##folder containing gene trees that failed TOAST genetrees_TOAST_pass ##folder containing gene trees that passed TOAST and lack odd long branches TOAST_fail_weird_branches ##folder containing gene trees that failed TOAST and have odd long branches tree_trim_sheet.xlsx ##record sheet Singleton_Bad_long_branches ##list of taxa that have odd long branches subtending them in one tree Multiple_bad_long_branches ##list of taxa that have odd long branches subtending them in many trees Desktop\omit_trees.csv ##list of trees to omit

SSE.zip ## Data for state dependent diversification rate analyses Angler_MuSSE_reproduction.csv #reproductive traits Angler_BiSSE_locomotion.csv #locomotion traits Angler_BiSSE_reproduction_2.csv #reproduction traits 2 Angler_MuSSE_habitat.csv #MuSSE reproducion

xmls_corrected.zip ##XML files for the 15 largest partitions; see main text for prior specs

logs.zip ##log file output for the 11 converged BEAST runs

Top_11_SUM.trees ##combined posterior trees file for 11 converged BEAST runs

IQTREE_Basis.tree ##target tree without branch lengths (partitioned IQ TREE topology)

BEAST_Sum.tree ##summary tree from BEAST

Individuals_for_BEAST.xlsx ##BEAST individuals file

Supplementary_Figures.pdf ##PDF containing Supplementary Figures.

Supplementary_Figure_Captions.docx ##Supplementary Figure Captions

BioSampleObjects.txt ##Genbank BioObjects File for UCE Data

Code/Software

All code is contained in : Anglerfish_Script_R.R

Log Changes:

Dec 25, 2024: Changed title to match final title of published manuscript

Synergistic innovations enabled the radiation of anglerfishes in the deep open ocean

Data files

Abstract

README: Reproductive innovation enabled radiation in the deep sea during an ecological crisis

Description of the data and file structure

Code/Software

Log Changes:

Methods

Works referencing this dataset