Consequences of Population Structure on Genes Under Balancing Selection

Abstract

Abstract. This paper describes a new approach to modeling population structure for genes under strong balancing selection of the type seen in plant self-incompatibility systems and the major histocompatibility complex (MHC) system of vertebrates. Simple analytic solutions for the number of alleles maintained at equilibrium and the expected proportion of alleles shared between demes at various levels are derived and checked against simulation results. The theory accurately captures the dynamics of allele number in a subdivided population and identifies important values of m (migration rate) at which allele number and distribution change qualitatively. Starting from a panmictic population, as migration among demes decreases a qualitative change in dynamics is seen at approximately m crit ഠ (s/4N T ) 1/2 , where N T is the total population size and s is a measure of the strength of selection. At this point, demes can no longer maintain their panmictic allele number, due to increasing isolation from the total population. Another qualitative change occurs at a migration rate on the same order of magnitude as the mutation rate, u. At this point, the demes are highly differentiated for allele complement, and the total number of alleles in the population is increased. Because in general u K m crit , at intermediate migration rates slightly fewer alleles may be maintained in the total population than are maintained at panmixia. Within this range, total allele number may not be the best indicator of whether a population is effectively panmictic, and some caution should be used when interpreting samples from such populations. The theory presented here can help to analyze data from genes under balancing selection in subdivided populations.

Effect of balancing selection on spatial genetic structure within populations: theoretical investigations on the self-incompatibility locus and empirical studies in Arabidopsis halleri

“…Previous studies had shown that under restricted dispersal, patterns of SGS would develop at the S-locus (Brooks et al, 1996;Neuhauser, 1999;Cartwright, 2009), but they did not explicitly compare those with SGS at unlinked neutral loci. Our study results thus constitute an extension of the theoretical results obtained in island models of subdivided populations, for which a substantially lower level of genetic differentiation was found among populations at the S-locus as compared with unlinked neutral loci (Schierup et al, 2000;Muirhead, 2001). These predictions were interpreted as resulting from an increase in the effective migration rate at the S-locus due to frequency-dependent selection.…”

“…This phenomenon causes a higher 'effective migration rate' (Barton and Bengtsson, 1986) at the S-locus as compared to neutral genes. A low population genetic structure at the S-locus is thus expected, even under very restricted migration (Schierup et al, 2000;Muirhead, 2001). These predictions have been tested in natural populations, and the results showed that the S-locus has indeed a lower genetic differentiation among populations than neutral loci (Glémin et al, 2005;Schierup et al, 2008;Stoeckel et al, 2008).…”

“…Increased differentiation at selected loci has been documented associated with local adaptation, as for instance, the polymorphism of the lactase-persistence gene in humans (Burger et al, 2007). In contrast, balancing selection is expected to reduce the extent of genetic differentiation among populations (Charlesworth et al, 1997;Schierup et al, 2000;Muirhead, 2001).…”

Detecting population structure in a high gene-flow species, Atlantic herring (Clupea harengus): direct, simultaneous evaluation of neutral vs putatively selected loci

“…However, with the exception of a precursory characterization of the MHC class IIA gene and an embedded microsatellite locus in Atlantic herring (Stet et al, 2008), no studies exist to date that describe the MHC variation in an abundant and fully marine fish. It is worth noting, however, that divergence in genes under selection is not always expected; if fish populations share similar parasite environments, balancing selection can result in lower levels of differentiation in MHC-linked microsatellites than neutral microsatellites (Muirhead, 2001;Bernatchez and Landry, 2003).…”

Impact of negative frequency-dependent selection on mating pattern and genetic structure: a comparative analysis of the S-locus and nuclear SSR loci in Prunus lannesiana var. speciosa

“…Thus, a greater number of alleles are expected at the S-locus than at selectively neutral loci. Several theoretical studies have predicted that the patterns of polymorphism among populations are different between genes subject to NFDS and selectively neutral loci (Schierup, 1998;Schierup et al, 2000;Muirhead, 2001). NFDS that favors rare migrant alleles is expected to increase effective migration rates, so that the alleles tend to be shared among populations.…”