From coral reefs into the abyss: the evolution of corallivory in the Coralliophilinae (Neogastropoda, Muricidae)

Abstract

In this study, we delved into the interaction between corallivorous marine gastropods, the muricid Coralliophilinae Chenu, 1859, and their cnidarian food targets. Coralliophilinae is a subfamily of specialised corallivorous caenogastropods that feed by browsing on octocorals or hexacorals. Only sparse information is available on the phylogenetic relationships and the degree of specificity of the trophic relationships within this corallivorous lineage. To address these gaps, we generated the largest molecular dataset to date, comprising two mitochondrial (cox1 and 16S rDNA) and one nuclear gene (ITS2 rDNA) from 586 specimens collected worldwide. The coral hosts of coralliophilines were identified through an integrative approach, combining literature data with new records, employing morphological and/or molecular markers, and incorporating data from DNA barcoding of the snail stomach content. Our comprehensive approach unveiled the existence of numerous cryptic species in Coralliophilinae, while the phylogeny showed that most of the currently accepted genera are not monophyletic. The molecular dating confirmed the origin of the Coralliophilinae in Middle Eocene, with diversification of most lineages during the Miocene. Our results indicate that the subfamily's ancestor evolved in shallow waters in association with Scleractinia. Through the evolutionary history of Coralliophilinae, multiple host shifts to other cnidarian orders were observed, not correlated with changes in the depth range. The results of diversification analyses within the subfamily further suggest that the association with the host has influenced the evolutionary patterns of Coralliophilinae, but not vice versa.

Supplementary information: The online version contains supplementary material available at 10.1007/s00338-024-02537-1.

Keywords: Cnidaria; Coevolution; Corallivory; Gastropods; Host–parasite interactions; Molecular phylogeny.

Fig. 1

Living specimens of coralliophiline species on their hosts. a Galeropsis monodontus on Pocilloporidae, Papua New Guinea. b Coralliophila radula on Poritidae, New Caledonia. c Coralliophila rubrococcinea on Gorgoniidae, Philippines. d Coralliophila violacea on Poritidae, Kenya. e Coralliophila meyendorffii on Parazoanthidae, Italy. f Leptoconchus sp. in Merulinidae, Vanuatu. g Leptoconchus sp. in Fungiidae, Vanuatu. Photograph credits: a Laurent Charles (MNHN); b Philippe Maestrati (MNHN); c Guido Poppe (http://www.www.poppe-images.com); d–e Paolo Mariottini (University of Roma Tre); f–g Anne-Lise Fleddum (MNHN)

Fig. 2

Global map featuring sampling locations of the Coralliophilinae dataset created using QGIS. See Table S1 for corresponding locality identifiers

Fig. 3

Phylogenetic relationships of the subfamily Coralliophilinae (maximum likelihood tree on combined dataset), with clades collapsed by species. Numbers at nodes indicate branch support values [ultrafast bootstrap (Ufb) values and posterior probability (PP), respectively]; support values are shown only when at least one of them is ≥ 95%; black circles at nodes indicate maximum support (Ufb = 100, PP = 1). Photograph credits: Mélanie Van Weddingen (MNHN)

Fig. 4

Time calibrated, single species phylogenetic reconstruction obtained using BEAST on combined dataset. Bars at nodes indicate 95% confidence intervals of ages, expressed in mya. Asterisks (and numbers in bold) indicate the nodes (and the relevant fossil-based datings) used to time-calibrate the tree

Fig. 5

Diversification rates variation within Coralliophilinae across clades and time. a The single BAMM credible shifts plot representing the rate shift configuration and a posterior probability shift configuration corresponding to 1. b BAMM plot depicting the net diversification rates through time

Fig. 6

Graphical representation of the ancestral state reconstruction at each node of the phylogeny of the subfamily Coralliophilinae obtained from RASP by BBM analysis using depth range as a prior. Pie charts at each node (from 124 to 222) show the probabilities of alternative ancestral states; numbers inside the pie charts identify each node. The legend shows the colour key to the depth range. X-axis represents time in millions of years

Fig. 7

Graphical representation of the ancestral state reconstruction at each node of the phylogeny of the subfamily Coralliophilinae obtained from RASP by BBM analysis using cnidarian families as a prior. Pie charts at each node (from 124 to 222) show the probabilities of alternative ancestral states; numbers inside the pie charts identify each node. The legend shows the colour key to the hosts; black represents other unknown ancestral states. White barred circles represent no host information. X-axis represents time in millions of years

Fig. 8

Graphical representation of ancestral state reconstruction at each node of the phylogeny of the subfamily Coralliophilinae obtained from RASP by BBM analysis cnidarian orders as a prior. Pie charts at each node (from 124 to 222) show the probabilities of alternative ancestral states; numbers inside the pie charts identify each node. The legend shows the colour key to the hosts; black represents other unknown ancestral states. White barred circles represent no host information. X-axis represents time in millions of years