Genetic investigation of mouth asymmetry and lateralized (handed) foraging behavior in the scale-eating cichlid fish, Perissodus microlepis, from Lake Tanganyika, Africa
Final Report Abstract
Morphological variation plays a crucial role in the ecology and evolution of natural populations. One particularly interesting form morphological variation is polymorphisms: in this case - left-right asymmetry, where individuals within a species conspicuously differ in their bilateral symmetry. The scale-eating cichlid fish species, Perissodus microlepis, endemic to Lake Tanganyika has attracted much attention from evolutionary biologists since the ecological effects of the relative stable frequencies of both lateralized mouth morphs (they became a textbook example for negative -frequency dependent selection) were first documented in a publication by Hori in Science in 1993. This species comes in two morphs: one with a mouth that is turned to the right ('right' morph) and the other with a mouth that is directed towards the left ('left' morph). This mouth asymmetry is strongly associated with lateralized (handed) foraging behavior in that right morphs preferentially scrape scales from the left flanks of prey fish while left morphs forage from the right flanks. However, the ontogenetic mechanisms that determine the mouth asymmetry, lateralized foraging behavior and the forces that drive the co-evolution of these morphological and behavioral traits remain largely unknown. The proposed research had three main goals to determine: (1) the extent, bimodality and ontogenetic timing of mouth asymmetry in P. microlepis, (2) the genetic basis of mouth asymmetry and (3) the effect of phenotypic plasticity on mouth asymmetry and handed foraging behavior. This project made important contribution to a better understanding of this system, as we could show that: 1. The mouth asymmetry is not as bimodal and as distinct as thought before. 2. The behavioral laterality is rather pronounced and occurs early on in ontogeny and might in fact might be "driving" subsequent morphological asymmetry). 3. Although we could not concisely determine what the genetic component of head-laterality is, we could rule out an earlier hypothesis about the genetic basis of asymmetry. Moreover, we found some genomic signature that is associated with the asymmetric phenotype. This initial result was followed up on through more extensive sampling in the Northern region of Lake Tanganyika an a ddRADseq analysis. 4. As part of the genetic work to determine the heritability of the head asymmetry we conducted paternity analyses and discovered a surprising amount of alloparental care for offspring of other parents. This result was exciting, but was part of the reasons for the difficulties to investigate the genetics of this trait further. 5. We conducted a transcriptomic analysis (RNAseq) on preferentially left and right-attacking fish. Following a behavioral characterization we analyzed expression differences and found that, indeed, between preferentially right or left attacking fish there are significant differences in some regions of the brain.
Publications
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(2018) Gene(s) and individual feeding behavior: Exploring eco-evolutionary dynamics underlying left-right asymmetry in the scale-eating cichlid fish Perissodus microlepis. Ecology and evolution 8 (11) 5495–5507
Raffini, Francesca; Fruciano, Carmelo; Meyer, Axel
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(2012). Handed foraging behavior in scale-eating cichlid fish: Its potential role in shaping morphological asymmetry. PLoS ONE 7(9): e44670
Lee H.-J., Kusche H, and A. Meyer
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(2012). Mouth asymmetry in the textbook example of scaleeating cichlid fish is not a discrete dimorphism after all. Proceedings of the Royal Society B. 279: 4715-4723
Kusche H., Lee H.-J., and A. Meyer
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(2015). Genetic and environmental effects on the morphological asymmetry in the scale-eating cichlid fish Perissodus microlepis. Ecology & Evolution 5: 2045-7758
Lee H-J., Heim V., and A. Meyer
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(2016). Genetic evidence for prevalence of alloparental care in a socially monogamous biparental cichlid fish, Perissodus microlepis, from Lake Tanganyika supports the "selfish shepherd effect" hypothesis. Ecology & Evolution 6: 2843-2853
Lee H.-J., Heim V., and A. Meyer
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(2017). On the genetic basis of mouth asymmetry in the scale-eating cichlid fish Perissodus microlepis. Molecular Ecology 26: 77-91
Raffini, F., Fruciano, C., Franchini P. and A. Meyer
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(2017): Lateralized Feeding Behavior is Associated with Asymmetrical Neuroanatomy and Lateralized Gene Expressions in the Brain in Scale-Eating Cichlid Fish. In: Genome Biol Evol 9 (11), S. 3122–3136. DOI: 10.1093/gbe/evx218
Lee H.-J., Manousaki T., Kang J.H., Lein E., Franchini P., and A. Meyer