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Gene and allele specific expression during electric organ ontogeny in African weakly electric fish and hybrid

ABSTRACT: Hybridization can act as a catalyst for rapid phenotypic evolution by introducing novel allelic combinations, which can affect hybrid phenotype through changes in gene expression. The African weakly electric fish use their muscle-derived electric organ to produce electric organ discharge (EOD) for electrocommunication and electrolocation. The EOD in genus Campylomormyrus and cross-species hybrids is usually species-specific and varies during ontogeny. We compared the gene expression patterns and allele specific expression between juvenile and adult individuals in C. compressirostris (EOD duration 0.4 ms in juvenile and 0.4 ms in adult), C. rhynchophorus (EOD duration 5 ms in juvenile and 40 ms in adult) and their hybrid (EOD duration 0.4 ms in juvenile and 4 ms in adult). Differentially expressed genes between juveniles and adults were highly enriched in “membrane”, “plasma membrane” and “cytoplasm” Go Ontogeny terms. We detected several potassium channel-related genes (e.g. KCNJ2, ADCYAP1) that are potentially involved in the EOD development during ontogeny. The alleles from C. compressirostris show dominant expression in the hybrid at juvenile and adult life stages. KCNJ2 is the only gene that exhibits allelic dominance of C. rhynchophorus allele, and has an increasing expression during ontogeny in this allele. This suggests that the EOD development in hybrids could be related to the increasing allelic expression of the C. rhynchophorus allele under the scenario of overall dominance of C. compressirostris alleles. Our study sheds light in the evolution of the electric organ discharge in electric fishes and on the role of introgressive hybridization in complex phenotypic traits.

ORGANISM(S): Campylomormyrus compressirostris x Campylomormyrus rhynchophorus Campylomormyrus rhynchophorus Campylomormyrus compressirostris

PROVIDER: GSE240784 | GEO | 2023/08/31

REPOSITORIES: GEO

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Project description:Electric fishes have independently evolved six times. Most of these fish are weakly electric and they use their discharge mainly for orientation and communication. In the African weakly electric fish genus Campylomormyrus, electric organ discharge (EOD) signals are strikingly different in shape and duration among closely related species, they contribute to pre-zygotic isolation and may have triggered an adaptive radiation. We performed mRNA sequencing on electric organs (EOs) and skeletal muscle (SMs; from which the EOs derive) from three species with short (0.4 ms), medium (5 ms), and long (40 ms) EODs and two different cross-species hybrids. Using pairwise comparison of differential gene expression between EOs and SMs, we identified 1,444 up regulated genes in EO shared by all five species/hybrids cohorts, rendering them candidate genes for EO-specific properties in Campylomormyrus. To understand how gene expression contributes to the variation in EOD duration, we made cross species comparisons among species and tissue. We identified three types of EOD-duration-related expression patterns and several candidate genes, including KCNJ2, KLF5 and SLC24a2, their upregulation may contribute to increased EOD duration, along with a down-regulated gene KCNK6. Hybrids between a short (C. compressirostris) and a long (C. rhynchophorus) discharging species exhibit EODs of intermediate duration and showed imbalanced expression of KCNJ2 alleles. The preferential expression of the C. rhynchophorus allele is in line with a higher expression level in that parental species and points towards a cis-regulatory difference at this locus, relative to EOD duration. A further candidate gene, KLF5, is a transcription factor potentially balancing potassium channel gene expression, a crucial process for the formation of an EOD. Unraveling the genetic basis of the species-specific modulation of the EOD in Campylomormyrus is crucial for understanding the adaptive radiation of this emerging model taxon of ecological (perhaps even sympatric) speciation.

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Gene and allele specific expression during electric organ ontogeny in African weakly electric fish and hybrid

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