Complete genetic linkage can subvert natural selection

doi:10.1073/pnas.0607280104

Complete genetic linkage can subvert natural selection

^†Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, NM 87501;
^‡Instituto de Ecologia, Universidad Autónoma Nacional de México, Apartado Postal 70-275, Ciudad Universitaria, 04510 Distrito Federal, México;
^¶Instituto de Física de São Carlos, Universidade de São Paulo, Caixa Postal 369, 13560-970 São Carlos SP, Brazil;
^‖Theoretical Biology and Biophysics, Mail Stop K710, Los Alamos National Laboratory, Los Alamos, NM 87545; and
^††Department of Biology, University of Pennsylvania, Leidy Laboratories, 415 South University Avenue, Philadelphia, PA 19104

Edited by Tomoko Ohta, National Institute of Genetics, Mishima, Japan, and approved February 16, 2007 (received for review August 22, 2006)

Abstract

The intricate adjustment of organisms to their environment demonstrates the effectiveness of natural selection. But Darwin himself recognized that certain biological features could limit this effectiveness, features that generally reduce the efficiency of natural selection or yield suboptimal adaptation. Genetic linkage is known to be one such feature, and here we show theoretically that it can introduce a more sinister flaw: when there is complete linkage between loci affecting fitness and loci affecting mutation rate, positive natural selection and recurrent mutation can drive mutation rates in an adapting population to intolerable levels. We discuss potential implications of this finding for the early establishment of recombination, the evolutionary fate of asexual populations, and immunological clearance of clonal pathogens.

Footnotes

^§To whom correspondence should be addressed. E-mail: pgerrish{at}unm.edu
Author contributions: P.J.G., A.S.P., and P.D.S. designed research; P.J.G. and A.C. performed research; P.J.G. and A.S.P. contributed new reagents/analytic tools; P.J.G. and A.C. analyzed data; and P.J.G., A.S.P., and P.D.S. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
This article contains supporting information online at www.pnas.org/cgi/content/full/0607280104/DC1.