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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Albertson, R. C., Cresko, W., Detrich, H. W., & Postlethwait, J. H. (2008). Evolutionary mutant models for human disease. Trends in Genetics: TIG, 25(2), 74–81. doi:10.1016/j.tig.2008.11.006.
Albertson, R. C., & Kocher, T. D. (2001). Assessing morphological differences in an adaptive trait: A landmark-based morphometric approach. The Journal of experimental zoology, 289(6), 385–403. doi:10.1002/jez.1020.
Albertson, R. C., Streelman, J. T., & Kocher, T. D. (2003). Genetic basis of adaptive shape differences in the cichlid head. Journal of Heredity, 94(4), 291–301. doi:10.1093/jhered/esg071.
Albertson, R. C., Streelman, J. T., Kocher, T. D., & Yelick, P. C. (2005). Integration and evolution of the cichlid mandible: The molecular basis of alternate feeding strategies. Proceedings of the National Academy of Sciences of the United States of America, 102(45), 16287–16292. doi:10.1073/pnas.0506649102.
Arends, D., Prins, P., Broman, K., & Jansen, R. (2010). Tutorial-Multiple-QTL Mapping (MQM) Analysis. 1–39. Retrieved from http://rqtl.org/tutorials/MQM-tour.pdf.
Broman, K. W., & Sen, S. (2009). A guide to QTL mapping with R/qtl. Dordrecht, Heidelberg, London, New York: Springer. ISBN 987-0-387-92124-2.
Cooper, W. J., Parsons, K., McIntyre, A., Kern, B., McGee-Moore, A., & Albertson, R. C. (2010). Bentho-pelagic divergence of cichlid feeding architecture was prodigious and consistent during multiple adaptive radiations within African rift-lakes. PLoS ONE, 5(3), e9551. doi:10.1371/journal.pone.0009551.
Danley, P. D., & Kocher, T. D. (2001). Speciation in rapidly diverging systems: Lessons from Lake Malawi. Molecular Ecology, 10(5), 1075–1086. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/11380867.
Hallgrímsson, B., & Hall, B. K. (2005). Variation and variability: Central concepts in biology. In B. Hallgrímsson & B. K. Hall (Eds.), Variation: A central concept in biology B (pp. 1–7). New York: Academic Press.
Hallgrímsson, B., Jamniczky, H., Young, N. M., Rolian, C., Parsons, T. E., Boughner, J. C., et al. (2009). Deciphering the palimpsest: Studying the relationship between morphological integration and phenotypic covariation. Evolutionary Biology, 36(4), 355–376. doi:10.1007/s11692-009-9076-5.
Klingenberg, C. P. (2008). Morphological integration and developmental modularity. Annual Review of Ecology Evolution and Systematics, 39(1), 115–132. doi:10.1146/annurev.ecolsys.37.091305.110054.
Klingenberg, C. P. (2010). Evolution and development of shape: Integrating quantitative approaches. Nature Reviews Genetics, 11(9), 623–635. doi:10.1038/nrg2829.
Konings, A. (2001). Malawi cichlids in their natural habitat. El Paso, TX: Cichlid.
Marroig, G., & Cheverud, J. (2005). Size as a line of least evolutionary resistance: diet and adaptive morphological radiation in New World monkeys. Evolution, 59(5), 1128–1142. Retrieved from http://onlinelibrary.wiley.com/doi/10.1111/j.0014-3820.2005.tb01049.x/abstract.
Mayr, E. (1954). Change of genetic environment and evolution. In J. Huxley, A. C. Hardy, & E. B. Ford (Eds.), Evolution as a process (pp. 157–180). London: Allen & Unwin.
Olson, E. C., & Miller, R. L. (1958). Morphological integration. Chicago: University of Chicago Press.
Parsons, K. J., Cooper, W. J., & Albertson, R. C. (2011). Modularity of the oral jaws is linked to repeated changes in the craniofacial shape of African cichlids. International Journal of Evolutionary Biology, 2011, 641501. doi:10.4061/2011/641501.
Parsons, K. J., Márquez, E., & Albertson, R. C. (2012). Constraint and opportunity: The genetic basis and evolution of modularity in the cichlid mandible. The American Naturalist, 179(1), 64–78. doi:10.1086/663200.
Pavlicev, M., Cheverud, J. M., & Wagner, G. P. (2009). Measuring morphological integration using eigenvalue variance. Evolutionary Biology, 36(1), 157–170. doi:10.1007/s11692-008-9042-7.
Pigliucci, M., & Preston, K. (Eds.). (2004). Phenotypic integration: Studying the ecology and evolution of complex phenotypes. New York: Oxford University Press.
Ribbink, A. J., Marsh, B. A., Marsh, A. C., Ribbink, A. C., & Sharp, B. J. (1983). A preliminary survey of the cichlid fishes of rocky habitats in Lake Malawi. South African Journal of Zoology, 18(3), 149–309.
Rosas-Guerrero, V., Quesada, M., Armbruster, W. S., Pérez-Barrales, R., & Smith, S. D. (2011). Influence of pollination specialization and breeding system on floral integration and phenotypic variation in Ipomoea. Evolution; International Journal of Organic Evolution, 65(2), 350–364. doi:10.1111/j.1558-5646.2010.01140.x.
Rowe, H. C., Renaut, S., & Guggisberg, A. (2011). RAD in the realm of next-generation sequencing technologies. Molecular Ecology, 20(17), 3499–3502. PubMed PMID: 21991593.
Schluter, D. (1996). Adaptive radiation along genetic lines of least resistance. Evolution, 50(5), 1766–1774. Retrieved from http://www.jstor.org/stable/10.2307/2410734.
Streelman, J. T., Albertson, R. C., & Kocher, T. D. (2007). Variation in body size and trophic morphology within and among genetically differentiated populations of the cichlid fish, Metriaclima zebra, from Lake Malawi. Freshwater Biology, 52, 525–538. doi:10.1111/j.1365-2427.2006.01720.x.
Turner, G. F., Seehausen, O., Knight, M. E., Allender, C. J., & Robinson, R. L. (2001). How many species of cichlid fishes are there in African lakes? Molecular Ecology, 10(3), 793–806.
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.
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