Ecological interactions and genomic innovation fueled the evolution of ray-finned fish endothermy

Abstract

Endothermy has independently evolved in several vertebrate lineages but remains rare among fishes. Using an integrated approach combining phylogenomic and ecomorphological data for 1051 ray-finned fishes, a time-dependent evolutionary model, and comparative genomic analyses of 205 marine vertebrates, we show that ecological interactions with modern cetaceans coincided with the evolution of endothermy in ray-finned fishes during the Eocene-Miocene. This result is supported by evidence of temporal and geographical overlap between cetaceans and endothermic fish lineages in the fossil record, as well as correlations between cetacean diversification and the origin of endothermy in fishes. Phylogenetic comparative analyses identified correlations between endothermy, large body sizes, and specialized swimming modes while challenging diet specialization and depth range expansion hypotheses. Comparative genomic analyses identified several genes under selection in endothermic lineages, including carnmt1 (involved in fatty acid metabolism) and dcaf6 (associated with development). Our findings advance the understanding of how ecological interactions and genomic factors shape key adaptations.

Fig. 1.. Time tree of 1051 species of ray-finned fishes.

Tree based on 1099 single-copy nuclear exon markers. Colored fish illustrations indicate endothermic lineages, whereas grayscale illustrations represent their ectothermic counterparts. Colored dashed lines indicate endothermic lineages and the type of endothermy they exhibit. Colored branches show net diversification rates for all 1051 species, estimated using HiSSE. The central graph compares the distribution of diversification rates between endothermic and ectothermic ray-finned fishes. Illustration(s) by Julie Johnson (Life Science Studios).

Fig. 2.. Evolutionary correlations and tests for ecological interactions.

(A) Results illustrating nine sets of boxplots, each representing either one of the factors previously associated with the evolution of endothermy (white shaded) or one of the statistically significant factors obtained using additional morphometric traits (FS dataset) (blue shaded). The vertical dashed line represents the threshold for statistical significance (P value of 0.05). The vertical axis indicates whether the analysis was performed on a single trait (uv) or considering all traits jointly (mr). Each boxplot encompasses the distribution of the results of the PGLR analyses for the 19 different trees estimated to account for phylogenetic uncertainty. (B) LTT plots for all cetacean groups combined (Neoceti), Odontoceti, Mysticeti, and Carcharhiniformes, based on previously published phylogenies that include fossil and extant species. The vertical lines intersecting the LTT plots denote the origin of endothermic fish lineages. (C) AICw comparisons between our calibrated phylogeny (unmodified) and our artificially modified ages for the origin of endothermy (25 and 50% younger) for all four major ray-finned fish groups. Artificially modified ages accounted for any positive correlation biases introduced by our model or curves. Phylogenies on the right side of the panel illustrate the temporal differences in the origin of endothermy among the trees used. BM, Brownian motion; EB, Early Burst; LA, Pagel’s Lambda; OU, Ornstein-Uhlenbeck. Illustration(s) by Julie Johnson (Life Science Studios).

Fig. 3.. Fossil evidence of geographic coexistence between cetaceans and fishes.

Fossil record representations showing the geographical coexistence among different groups of predators and prey, suggesting potential ecological interactions among them. Major predators, alongside their correlated prey, were selected. Fossilized prey was included to support the observed geographical link to dietary ones, reinforcing the likelihood of such ecological interactions taking place. Each map represents intervals of 10 up to ~40 Myr, with dots indicating fossil location. Only regions with the simultaneous presence of at least four of our six fossil lineages are illustrated to maintain figure clarity. The intervals above the map indicate the fossil range age, and the number next to the silhouettes shows the fossils for each group and time range. Illustration(s) by Julie Johnson (Life Science Studios).

Fig. 4.. Positive selection of endothermic genes.

Genes that exhibited positive selection and accelerated relative rates of evolution across different scenarios using BUSTED-PH (corrected with BUSTED-E) and “RER.” The genes with the highest evolutionary rate for each scenario are underlined. Genes showing convergent signals are marked with an asterisk (*). Each scenario highlights the vertebrates used as the foreground species. We also highlighted regions used for internal heat production associated with genes under selection. The scenarios are (A) all endothermic species (foreground or fg) compared to all ectothermic species (background or bg), (B) regional endotherms (fg), all ectotherms (bg), and the other endothermic representatives as nuisance species, (C) eye/brain endotherms (fg), all ectotherms (bg), and the other endothermic representatives as our nuisance species, and (D) full-body endotherms (fg), all ectotherms (bg), and the other endothermic representatives as our nuisance species. (E) Upset plot indicating the number of genes under positive selection for each scenario. Boxes with black dots joined by a black line represent the number of genes shared between those highlighted scenarios. Although shared genes were observed among all endothermic species, some genes showing signatures of selection and accelerated evolution were found exclusively in some scenarios. Functional categories based on Biological Processes were obtained using the PANTHER database. Illustration(s) by Julie Johnson (Life Science Studios).