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Ecotype differences in aggression, neural activity and behaviorally relevant gene expression in cichlid fish.

ABSTRACT: In Lake Malawi, two ecologically distinct lineages of cichlid fishes (rock- vs sand-dwelling ecotypes, each comprised of over 200 species) evolved within the last million years. The rock-dwelling species (Mbuna) are aggressively territorial year-round and males court and spawn with females over rocky substrate. In contrast, males of sand-dwelling species are not territorial and instead aggregate on seasonal breeding leks in which males construct courtship "bowers" in the sand. However, little is known about how phenotypic variation in aggression is produced by the genome. In this study, we first quantify and compare behavior in seven cichlid species, demonstrating substantial ecotype and species differences in unconditioned mirror-elicited aggression. Second, we compare neural activity in mirror-elicited aggression in two representative species, Mchenga conophoros (sand-dwelling) and Petrotilapia chitimba (rock-dwelling). Finally, we compare gene expression patterns between these two species, specifically within neurons activated during mirror aggression. We identified a large number of genes showing differential expression in mirror-elicited aggression, as well as many genes that differ between ecotypes. These genes, which may underly species differences in behavior, include several neuropeptides, genes involved in the synthesis of steroid hormones and neurotransmitter activity. This work lays the foundation for future experiments using this emerging genetic model system to investigate the genomic basis of evolved species differences in both brain and behavior.

SUBMITTER: Baran NM

PROVIDER: S-EPMC7402082 | biostudies-literature | 2020 Jul

REPOSITORIES: biostudies-literature

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Ecotype differences in aggression, neural activity and behaviorally relevant gene expression in cichlid fish.

Baran Nicole M NM Streelman J Todd JT

Genes, brain, and behavior 20200508 6

In Lake Malawi, two ecologically distinct lineages of cichlid fishes (rock- vs sand-dwelling ecotypes, each comprised of over 200 species) evolved within the last million years. The rock-dwelling species (Mbuna) are aggressively territorial year-round and males court and spawn with females over rocky substrate. In contrast, males of sand-dwelling species are not territorial and instead aggregate on seasonal breeding leks in which males construct courtship "bowers" in the sand. However, little is ...[more]

PMID: 32323443

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Project description:Purpose: The goal of this study is to identify genes that showed a pattern of differential expression between species within activated neurons during mirror-elicited aggression between two species of Lake Malawi cichlid fish which differ in aggressive behaviors, Mchenga conophoros (MC, sand-dwelling) and Petrotilapia chitimba (PC, rock-dwelling). To do this, we use antibodies to phosphorylated ribosomal protein S6 (pS6) to enrich for transcripts bound to phosphorylated ribosomes followed by RNA-seq (PhosphoTRAP). In neurons, this phosphorylation occurs downstream of the binding of neurotransmitters and, thus, pS6 antibodies are increasingly being used as markers of neural activity, similar to immediate early genes (IEGs) like c-fos or egr-1. Methods: Whole brain mRNA samples were collected from 8 adult male cichlids (4 MC, 4 PC) 90min following either 15min exposure to mirror in home tank (Mirror Test) or a Control condition. RNA-immunoprecipitation using antibodies to pS6 were performed and RNA was extracted from immunoprecipitated (IP) RNA samples. We also collected total RNA (input), prior to immunoprecipitation. For details see extraction protocol below. RNA from both input and IP samples was reverse transcribed using the SMART-Seq v4 Ultra Low Input RNA kit. Libraries were prepped using the NEBNext Ultra II FS DNA library Prep Kit for Illumina and sequenced. Sequence reads that passed quality filters were aligned to the Metriaclima zebra (Malawi cichlid) reference genome UMD2A using HiSat2. Transcripts were quantified using StringTie and differential expressional analyses were performed using DESeq2. Results: We identified a large number of genes showing differential expression in mirror-elicited aggression, as well as many genes that differ between ecotypes. These genes, which may underly species differences in behavior, include several neuropeptides, genes involved in the synthesis of steroid hormones, and neurotransmitter activity. Conclusions: This work lays the foundation for future experiments using this emerging genetic model system to investigate the genomic basis of evolved species differences in both brain and behavior.

Project description:Aggression is ubiquitous among social species and functions to maintains social dominance hierarchies. The African cichlid fish Astatotilapia burtoni is an ideal study species for studying aggression due to their unique and flexible dominance hierarchy. However, female aggression in this species and the neural mechanisms of aggression in both sexes is not well understood. To further understand the potential sex differences in aggression in this species, we characterized aggression in male and female A. burtoni in a mirror assay. We then quantified neural activation patterns in brain regions of the social behavior network (SBN) to investigate if differences in behavior are reflected in the brain with immunohistochemistry by detecting the phosphorylated ribosome marker phospho-S6 ribosomal protein (pS6), a marker for neural activation. We found that A. burtoni perform both identical and sex-specific aggressive behaviors in response to a mirror assay. We observed sex differences in pS6 immunoreactivity in the Vv, a homolog of the lateral septum in mammals. Males but not females had higher ps6 immunoreactivity in the ATn after the aggression assay. The ATn is a homolog of the ventromedial hypothalamus in mammals, which is strongly implicated in the regulation of aggression in males. Several regions also have higher pS6 immunoreactivity in negative controls than fish exposed to a mirror, implicating a role for inhibitory neurons in suppressing aggression until a relevant stimulus is present. Male and female A. burtoni display both similar and sexually dimorphic behavioral patterns in aggression in response to a mirror assay. There are also sex differences in the corresponding neural activation patterns in the SBN. In mirror males but not females, the ATn clusters with the POA, revealing a functional connectivity of these regions that is triggered in an aggressive context in males. These findings suggest that distinct neural circuitry underlie aggressive behavior in male and female A. burtoni, serving as a foundation for future work investigating the molecular and neural underpinnings of sexually dimorphic behaviors in this species to reveal fundamental insights into understanding aggression.

Project description:Neural crest (NC) is a vertebrate-specific embryonic progenitor cell population at the basis of important vertebrate features such as the craniofacial skeleton and pigmentation patterns. Despite the wide-ranging variation of NC-derived traits across vertebrates, the contribution of NC to species diversification remains underexplored. Here, leveraging the adaptive diversity of African Great Lakes' cichlid species, we combined comparative transcriptomics and population genomics to investigate the evolution of the NC genetic program in the context of their morphological divergence. Our analysis revealed substantial differences in transcriptional landscapes across somitogenesis, an embryonic period coinciding with NC development and migration. This included dozens of genes with described functions in the vertebrate NC gene regulatory network, several of which showed signatures of positive selection. Among candidates showing between-species expression divergence, we focused on teleost-specific paralogs of the NC-specifier sox10 (sox10a and sox10b) as prime candidates to influence NC development. These genes, expressed in NC cells, displayed remarkable spatio-temporal variation in cichlids, suggesting their contribution to interspecific morphological differences, such as craniofacial structures and pigmentation. Finally, through CRISPR/Cas9 mutagenesis, we demonstrated the functional divergence between cichlid sox10 paralogs, with the acquisition of a novel skeletogenic function by sox10a. When compared with teleost models zebrafish and medaka, our findings reveal that sox10 duplication, although retained in most teleost lineages, had variable functional fates across their phylogeny. Altogether, our study suggests that NC-related processes—particularly those controlled by sox10s—are involved in generating morphological diversification between species and lays the groundwork for further investigations into the mechanisms underpinning vertebrate NC diversification.

Dataset Information

Ecotype differences in aggression, neural activity and behaviorally relevant gene expression in cichlid fish.

Publications

Ecotype differences in aggression, neural activity and behaviorally relevant gene expression in cichlid fish.

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