Shared neural transcriptomic patterns underlie the repeated evolution of mutualistic cleaning behavior in Labridae wrasses

Abstract

Despite the remarkable diversity of life forms on earth, evolutionary biologists have discovered numerous instances where even distantly related species share astonishing similarities in how they behave, look, and function. Given the importance of happenstance in evolution (e.g., random mutations, genetic drift, environmental stochasticity), it is often assumed that the mechanisms underlying such convergent phenotypes are distinct. Nevertheless, recent discoveries that the same pathways can underlie convergently evolved phenotypes have reinvigorated questions about the predictability of evolution and whether broadly conserved genomic mechanisms facilitate phenotypic convergence. Here, we generated transcriptomes of the putative teleost homologs of the mammalian hippocampus and basolateral amygdala, broadly associated with spatial and social cognition, in six sympatric species of Labridae wrasses that vary in mutualistic cleaning behavior (including three non-cleaning, two facultative cleaning, and one obligate cleaning species) and combined differential gene expression, gene co-expression, and phylogenetic comparative analyses to test two hypotheses about convergent evolution and specialization of mutualistic cleaning behavior. We first identify genes and gene modules exhibiting parallel neurotranscriptomic patterns in the repeated evolution of facultative cleaning. We then examined whether expression and co-expression patterns associated with facultative cleaning are also shared in the obligate cleaner species in our dataset and found evidence for transcriptomic concordance, though no evidence for additional specialization. Taken together, our results provide insights into the convergent evolution and the neuromolecular basis of cooperative behavior and, more generally, illustrate the potential of phylogenetic comparative transcriptomics to unravel the mechanistic underpinnings of the repeated evolution of complex organismal phenotypes.

Mate choice in the brain: species differ in how male traits ‘turn on’ gene expression in female brains

“…This could have been either owing to the available genetic variants differing ( sensu the mutation order hypothesis [ 51 – 53 ]), or because selection was less similar than thought. Although there are exciting examples of parallel gene expression changes underlying the parallel evolution of complex behavioural phenotypes [ 11 – 14 , 33 ], it seems that parallel phenotypic evolution often rests on only partly parallel genetic mechanisms [ 31 , 54 ], as is suggested by the data from the two limnetic populations here.…”

“…However, we know little about the cognitive and molecular mechanisms that underpin such decision-making or how these mechanisms vary across species [ 9 , 10 ]. Comparative transcriptomic studies, where constitutive gene expression profiles are systematically analysed across different populations, species and environments, have already provided important insights into the evolution of molecular mechanisms underlying various complex behaviours, such as learned vocalizations [ 11 ], mating systems [ 12 , 13 ], and cooperation [ 14 ]. Recent studies have also identified dynamic transcriptomic variation related to mate choice [ 15 , 16 ].…”

Mate choice in the brain: Species differ in how male traits ‘turn on’ gene expression in female brains

“…This could have been either due to the available genetic variants differing ( sensu the mutation order hypothesis (Mani and Clarke 1997; Schluter 2009; Mendelson et al 2014)), or because selection was less similar than thought. Although there are exciting examples of parallel gene expression changes underlying parallel evolution of complex behavioral phenotypes (Pfenning et al 2014; Renn et al 2018; Young et al 2019; Jacobs et al 2020; Young et al 2022), it seems that parallel phenotypic evolution often rests on only partly parallel genetic mechanisms (Soria-Carrasco et al 2014; Bolnick et al 2018).…”

“…However, we know very little about the cognitive and molecular mechanisms that underpin such decision-making or how these mechanisms may vary across species and depend on ecological factors (DeAngelis and Hofmann 2020; Ryan 2021). Comparative transcriptomics, where gene expression profiles are systematically analyzed across different populations, species, and environments, have already provided important insights into the evolution of mechanisms underlying various complex behaviors, such as learned vocalizations (Pfenning et al 2014), mating systems (Renn et al 2018; Young et al 2019), and cooperation (Young et al 2022). Recent transcriptomic studies have also identified some genes that appear to be involved in female mate choice (Cummings et al 2008; Bloch et al 2018).…”

The cytoarchitecture of the telencephalon of Labroides dimidiatus (Labridae)

“…Young et al 2022;Kang et al 2023). The former analysis was based on two telencephalic nodes of the Social Decision-Making Network, the medial (Dl; lateral part of the dorsal telencephalon) and the lateral pallium (area Dm; medial part of the dorsal telencephalon).…”