Somewhere I belong: phylogeny and morphological evolution in a species‐rich lineage of ectoparasitic flatworms infecting cichlid fishes

Abstract

A substantial portion of biodiversity has evolved through adaptive radiation. However, the effects of explosive speciation on species interactions remain poorly understood. Metazoan parasites infecting radiating host lineages could improve our knowledge because of their intimate host relationships. Yet limited molecular, phenotypic and ecological data discourage multivariate analyses of evolutionary patterns and encourage the use of discrete characters. Here, we assemble new molecular, morphological and host range data widely inferred from a species-rich lineage of parasites (Cichlidogyrus, Platyhelminthes: Monogenea) infecting cichlid fishes to address data scarcity. We infer a multimarker (28S/18S rDNA, ITS1, COI mtDNA) phylogeny of 58 of 137 species and characterize major lineages through synapomorphies inferred from mapping morphological characters. We predict the phylogenetic position of species without DNA data through shared character states, a morphological phylogenetic analysis, and a classification analysis with support vector machines. Based on these predictions and a cluster analysis, we assess the systematic informativeness of continuous characters, search for continuous equivalents for discrete characters, and suggest new characters for morphological traits not analysed to date. We also model the attachment/reproductive organ and host range evolution using the data for 136 of 137 described species and multivariate phylogenetic comparative methods (PCMs). We show that discrete characters not only can mask phylogenetic signals, but also are key for characterizing species groups. Regarding the attachment organ morphology, a divergent evolutionary regime for at least one lineage was detected and a limited morphological variation indicates host and environmental parameters affecting its evolution. However, moderate success in predicting phylogenetic positions, and a low systematic informativeness and high multicollinearity of morphological characters call for a revaluation of characters included in species characterizations.

Explosive networking: The role of adaptive host radiations and ecological opportunity in a species‐rich host–parasite assembly

“…As no previous phylogenetic study covers all the species known to host members of Cichlidogyrus, we conducted a new analysis (see Appendix S2.1) based on sequence data of 11 nuclear and mitochondrial DNA regions accessed on GenBank (Appendix S3) to infer phylogenetic distances between host species. For the parasites, we included published morphometric and phylogenetic data, that is morphological measurements and 100 randomly sampled Bayesian tree topologies from the post-burn in fraction (Cruz-Laufer et al, 2022).…”

“…One such co-radiations was reported in species of Cichlidogyrus infecting tropheine cichlids in LT using a parasite lineage-through-time plot (Vanhove et al, 2015). However, a study of morphological characters detected no such pattern across the whole genus (Cruz-Laufer et al, 2022) leaving the question open whether the LT and LV lineages as a whole present parasite co-radiations.…”

Parasites (Monogenea) of tilapias Oreochromis niloticus and Coptodon rendalli (Cichlidae) in a river spring in Brazil

“…The representative sequences of Cichlidogyrus and Scutogyrus used in our analyses formed several supported/unsupported monophyletic groups, showing that the relationships between congeners are still unresolved and require further analyses. Cruz-Laufer et al [14] provided a phylogeny based on a four-locus multiple alignment (partial ITS1, SSU rDNA, LSU rDNA, and COI mtDNA sequence data) along with different comparative methods and parameters (see Cruz-Laufer et al [14] for specific methodology), which recovered similar topology compared to ours albeit with moderate to well-supported clades within Cichlidogyrus. This difference was probably generated by the increased set of molecular markers and methods used in those authors' analyses.…”

The role of systematics for understanding ecosystem functions: Proceedings of the Zoologica Scripta Symposium, Oslo, Norway, 25 August 2022

“…As an example of recent work in which systematic, genetic and ecological understanding of this cichlid‐monogenean model fed into each other, Cruz‐Laufer, Pariselle, et al (2022) provided an updated multimarker phylogeny of the lineage of Cichlidogyrus and Scutogyrus . Using this reconstruction in combination with machine learning, they assessed the diagnostic value, and use, of morphological characters and host repertoire data typically used for phenotyping and classifying these monogeneans.…”