Evolvability of the Cichlid Jaw: New Tools Provide Insights into the Genetic Basis of Phenotypic Integration

Abstract

Phenotypic integration is a phenomenon that manifests itself as the covariation among traits, and is thought to substantially influence how evolution unfolds, both in terms of rate and direction, which ultimately determines evolvability. To date little is known about how integration may change across an adaptive radiation, nor do we have a way of determining its genetic basis. Here we sought to test the hypotheses that (1) higher magnitudes of integration are associated with a greater degree of eco-morphological divergence, and (2) integration has a tractable genetic basis. To this end, we first evaluated the magnitude of integration at the population level in the lower jaws of two Lake Malawi cichlid species that exhibit different degrees of trophic specialization. We find that the more eco-morphologically divergent species does indeed exhibit a significantly higher magnitude of integration, which is consistent with our first hypothesis. Next, we developed a new statistical approach based on jackknife pseudovalues to produce a quantitative trait representative of inter-individual variation in the magnitude of integration. This metric was successfully applied to map the genetic basis of integration in the lower jaws of F2 hybrids derived from the two parental species that exhibited differences in the magnitude of integration. We detected three QTLs and two epistatic interactions that contribute to variation in integration within the cichlid mandible. We also detected a single QTL for lower jaw shape. None of the single QTLs for integration identified here overlapped with the interval for lower jaw shape, although one of the epistatic loci for integration did overlap with shape QTL. These results underscore a complex relationship between integration and shape, but suggest largely distinct genetic bases for these two traits. In all, our results show that phenotypic integration has a tractable, yet complex, genetic basis and that we now have the tools available to shed new light on the mechanisms that both promote and limit craniofacial diversity.

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Acknowledgments

We thank members of the Albertson lab and the Behavior and Morphology reading group at UMass for critical reading and feedback on this manuscript. This work was supported by an NSF grant (CAREER IOS-1054909) to R. C. A.

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Correspondence to R. Craig Albertson.

Appendix: R script for measuring magnitude of integration on individual-level

Appendix: R script for measuring magnitude of integration on individual-level

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Hu, Y., Parsons, K.J. & Albertson, R.C. Evolvability of the Cichlid Jaw: New Tools Provide Insights into the Genetic Basis of Phenotypic Integration. Evol Biol 41, 145–153 (2014). https://doi.org/10.1007/s11692-013-9254-3

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Keywords

  • Integration
  • QTL
  • Evolvability
  • Cichlid
  • Craniofacial