Gene losses, parallel evolution and heightened expression confer adaptations to dedicated cleaning behaviour
by Jingliang Kang | Sandra Ramirez-Calero | José Ricardo Paula | Yifang Chen | Celia Schunter | Swire Institute of Marine Science, School of Biological Science, The University of Hong Kong | Swire Institute of Marine Science, School of Biological Science, The University of Hong Kong, Pokfulam, Hong Kong SAR | MARE—Marine and Environmental Sciences Centre, Laboratório Marítimo da Guia, Faculdade de Ciências, Universidade de Lisboa | State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong | State Key Laboratory of Marine Pollution and Department of Chemistry, City University of Hong Kong
Abstract ID: 20
Event: The 3rd AsiaEvo Conference
Topic: The genomics of adaptation and speciation
Presenter Name: Jingliang Kang

Cleaning symbioses are captivating interspecific interactions in which a cleaner fish removes ectoparasites from its client, contributing to the health and diversity of natural fish communities and aquaculture systems. However, the genetic signatures underlying this specialized behaviour remain poorly explored. To shed light on this, we generated a high-quality chromosome-scale genome of the bluestreak cleaner wrasse Labroides dimidiatus, a dedicated cleaner with cleaning as primary feeding mechanism throughout its life. Compared with facultative and non-cleaner wrasses, L. dimidiatus was found with notable contractions in olfactory receptors implying their limited importance in dedicated cleaning. Instead, given its distinct tactile pre-conflict strategies, L. dimidiatus may rely more heavily on touch sensory perception, with heightened gene expression in the brain in anticipation of cleaning. Additionally, a reduction in NLR family CARD domain-containing protein 3 might enhance innate immunity of L. dimidiatus, probably assisting to reduce the impacts from parasite infections. In addition, convergent substitutions for a taste receptor and bone development genes across cleaners (L. dimidiatus and facultative cleaners) may provide them with evolved food discrimination abilities and jaw morphology that differentiate them from non-cleaners. Moreover, L. dimidiatus may exhibit specialized neural signal transductions for cleaning, as evidenced by positive selection in genes related to the glutamatergic synapse pathway. Interestingly, numerous glutamate receptors also demonstrated significantly higher expression in L. dimidiatus not engaged in cleaning, as compared to those involved in cleaning. Besides, apparent contractions in L. dimidiatus for protocadherins, which are responsible for neuronal development, may further promote specialised neural signal transductions in this species. This study reveals that L. dimidiatus harbours substantial losses in specific gene families, convergent evolutions across cleaners, and a large-scale high gene expression in preparation for cleaning, allowing for adaptation to the dedicated cleaning behaviour.