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Electrifying love: electric fish use species-specific discharge for mate recognition.

ABSTRACT: Mate choice is mediated by a range of sensory cues, and assortative mating based on these cues can drive reproductive isolation among diverging populations. A specific feature of mormyrid fish, the electric organ discharge (EOD), is used for electrolocation and intraspecific communication. We hypothesized that the EOD also facilitates assortative mating and ultimately promotes prezygotic reproductive isolation in African weakly electric fishes. Our behavioural experiments using live males as well as EOD playback demonstrated that female mate recognition is influenced by EOD signals and that females are attracted to EOD characteristics of conspecific males. The dual function of the EOD for both foraging and social communication (including mate recognition leading to assortative mating) underlines the importance of electric signal differentiation for the divergence of African weakly electric fishes. Thus, the EOD provides an intriguing mechanism promoting trophic divergence and reproductive isolation between two closely related Campylomormyrus species occurring in sympatry in the lower Congo rapids.

SUBMITTER: Feulner PG

PROVIDER: S-EPMC2665802 | biostudies-literature | 2009 Apr

REPOSITORIES: biostudies-literature

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Electrifying love: electric fish use species-specific discharge for mate recognition.

Feulner Philine G D PG Plath Martin M Engelmann Jacob J Kirschbaum Frank F Tiedemann Ralph R

Biology letters 20081125 2

Mate choice is mediated by a range of sensory cues, and assortative mating based on these cues can drive reproductive isolation among diverging populations. A specific feature of mormyrid fish, the electric organ discharge (EOD), is used for electrolocation and intraspecific communication. We hypothesized that the EOD also facilitates assortative mating and ultimately promotes prezygotic reproductive isolation in African weakly electric fishes. Our behavioural experiments using live males as wel ...[more]

PMID: 19033131

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Project description:African weakly electric fish of the mormyrid genus Campylomormyrus generate pulse-type electric organ discharges (EODs) for orientation and communication. Their pulse durations are species-specific and elongated EODs are a derived trait. So far, differential gene expression among tissue-specific transcriptomes across species with different pulses and point mutations in single ion channel genes indicate a relation of pulse duration and electrocyte geometry/excitability. However, a comprehensive assessment of expressed Single Nucleotide Polymorphisms (SNPs) throughout the entire transcriptome of African weakly electric fish, with the potential to identify further genes influencing EOD duration, is still lacking. This is of particular value, as discharge duration is likely based on multiple cellular mechanisms and various genes. Here we provide the first transcriptome-wide SNP analysis of African weakly electric fish species (genus Campylomormyrus) differing by EOD duration to identify candidate genes and cellular mechanisms potentially involved in the determination of an elongated discharge of C. tshokwe. Non-synonymous substitutions specific to C. tshokwe were found in 27 candidate genes with inferred positive selection among Campylomormyrus species. These candidate genes had mainly functions linked to transcriptional regulation, cell proliferation and cell differentiation. Further, by comparing gene annotations between C. compressirostris (ancestral short EOD) and C. tshokwe (derived elongated EOD), we identified 27 GO terms and 2 KEGG pathway categories for which C. tshokwe significantly more frequently exhibited a species-specific expressed substitution than C. compressirostris. The results indicate that transcriptional regulation as well cell proliferation and differentiation take part in the determination of elongated pulse durations in C. tshokwe. Those cellular processes are pivotal for tissue morphogenesis and might determine the shape of electric organs supporting the observed correlation between electrocyte geometry/tissue structure and discharge duration. The inferred expressed SNPs and their functional implications are a valuable resource for future investigations on EOD durations.

Project description:Sensory and social inputs interact with underlying gene suites to coordinate social behavior. Here we use a naturally complex system in sexual selection studies, the swordtail, to explore how genes associated with mate preference, receptivity, and social affiliation interact in the female brain under specific social conditions. We focused on 11 genes associated with mate preference in this species (neuroserpin, neuroligin-3, NMDA receptor, tPA, stathmin-2, ?-1 adrenergic receptor) or with female sociosexual behaviors in other taxa (vasotocin, isotocin, brain aromatase, ?-1 adrenergic receptor, tyrosine hydroxylase). We exposed females to four social conditions, including pairings of differing mate choice complexity (large males, large/small males, small males), and a social control (two females). Female mate preference differed significantly by context. Multiple discriminant analysis (MDA) of behaviors revealed a primary axis (explaining 50.2% between-group variance) highlighting differences between groups eliciting high preference behaviors (LL, LS) vs. other contexts, and a secondary axis capturing general measures distinguishing a non-favored group (SS) from other groups. Gene expression MDA revealed a major axis (68.4% between-group variance) that distinguished amongst differential male pairings and was driven by suites of "preference and receptivity genes"; whereas a second axis, distinguishing high affiliation groups (large males, females) from low (small males), was characterized by traditional affiliative-associated genes (isotocin, vasotocin). We found context-specific correlations between behavior and gene MDA, suggesting gene suites covary with behaviors in a socially relevant context. Distinct associations between "affiliative" and "preference" axes suggest mate preference may be mediated by distinct clusters from those of social affiliation. Our results highlight the need to incorporate natural complexity of mating systems into behavioral genomics.

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.

Dataset Information

Electrifying love: electric fish use species-specific discharge for mate recognition.

Publications

Electrifying love: electric fish use species-specific discharge for mate recognition.

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