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Functional and Genetic Integration in the Skulls of Lake Malawi Cichlids

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Abstract

The level of integration present among organismal traits is thought to influence evolutionary potential, and this potential should be affected by the type or types of integration displayed (e.g., functional, developmental, or genetic). Morphological integration is generally high among functionally related traits, but whether this is predominantly determined by genetic architecture, or is instead a result of biomechanical remodeling during development remains poorly understood. We examine this question in Lake Malawi cichlid fishes by combining a finite-element analysis (FEA) of bite force transmission with quantitative genetic analyses of skull morphology in order to test the hypothesis that functionally coupled traits share a common genetic basis. FEA modeling indicates that the profile of the neurocranium affects its ability to resist forces transmitted from the jaws during biting, and suggests a novel role for skull shape in fish feeding mechanics. Quantitative trait loci mapping demonstrates that the functional integration between jaw and neurocranial shape has a genetic basis, and that this association is being driven by alleles inherited from the specialized biting species. Notably, the co-inheritance of these two functionally related traits in our F2 matches patterns of covariation within and between Lake Malawi cichlid species. Across species, jaw and neurocranial shapes covary, but the trend appears strongest among biting species. Similarly, within populations of biting species, the dimensions of the jaw and neurocranium are tightly linked, whereas this correlation disappears within populations of omnivorous and suction feeding fish. These data suggest (1) that either pleiotropy, or physical linkage maintained by selection, underlies the phenotypic integration of these two functionally related traits, and (2) that this pattern of integration may have influenced the radiation of craniofacial morphology in Lake Malawi cichlids.

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Acknowledgments

We would like to thank J.T. Streelman and N. Parnell for providing the most recent Malawi cichlid linkage map for use in this study, and J.T. Streelman and E.R. Dumont for insightful comments on drafts of this manuscript.

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  1. R. Craig Albertson

    Present address: Department of Biology, University of Massachusetts Amherst, 611 North Pleasant Street, Amherst, MA, 01003, USA

Authors and Affiliations

  1. Department of Biology, Syracuse University, 107 College Place, Syracuse, NY, 13244, USA

    W. James Cooper & R. Craig Albertson

  2. Department of Orthopedic Surgery, 3216 Institute for Human Performance, SUNY Upstate Medical University, 750 East Adams Street, Syracuse, NY, 13210, USA

    James Wernle & Kenneth Mann

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Cooper, W.J., Wernle, J., Mann, K. et al. Functional and Genetic Integration in the Skulls of Lake Malawi Cichlids. Evol Biol 38, 316–334 (2011). https://doi.org/10.1007/s11692-011-9124-9

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