Multiple interacting loci control sex determination in lake Malawi cichlid fish

Abstract

Several models have been proposed to suggest how the evolution of sex-determining mechanisms might contribute to speciation. Here, we describe the inheritance of sex in 19 fish species from the rapidly evolving flock of cichlids in Lake Malawi, Africa. We found that many of these species have a male heterogametic (XY) system on linkage group 7. Some species also segregate for a female heterogametic (ZW) system on linkage group 5 that is coincident with a dominant orange-blotch (OB) color pattern in females. The ZW system is epistatically dominant to the XY system when both are segregating within a family. Several lines of evidence suggest that additional sex-determining loci are segregating in some species. These results are consistent with the idea that genetic conflicts play an important role in the evolution of these species flocks and suggest that evolution of sex-determining mechanisms has contributed to the radiation of cichlid fish in East Africa.

Figure 1

Metriaclima phaeos family (Meph-A006) showing segregation of an XY sex-determining locus on LG7. The two haplotypes of the dam are shown in shades of pink, those of the sire in blue. Numbers indicate the length of the microsatellite allele for each locus and zero indicates a null allele. The inferred genotype at the sex-determining locus is shown in the last column.

Figure 2

Metriaclima fainzilberi family (MeFaLI-A002) showing segregation of a ZW sex-determining locus on LG5. The two haplotypes of the dam are shown in shades of pink, those of the sire in blue. Numbers indicate the length of the microsatellite allele for each locus. The dam had a color phenotype of orange-blotch (OB), while the male had the standard blue-black (BB) color, and OB segregates as a dominant Mendelian allele tightly linked to gender. The inferred genotype at the sex-determining locus is shown in the last column.

Figure 3

Metriaclima pyrsonotus family (RMpy007) showing segregation of both a ZW sex determining locus on LG5 and an XY sex determining locus on LG7. The haplotypes of the dam on LG5 are shown in shades of pink. The haplotypes of the sire on LG7 are shown in blue. Numbers indicate the length of the microsatellite allele for each locus. The inferred genotypes at the two, epistatic, sex-determining loci segregating in this family are shown in the middle columns.

Figure 4

Summary of the diverse sex determining systems found in Lake Malawi cichlids. Symbols indicate the sex ratio of each family studied. Filled symbols indicate families genotyped for ma rkers on LG5 and LG7. Blue squares indicate families with a significant association for an XY sex-determining locus on LG7. Pink circles indicate families with a significant association with a ZW sex-determining locus on LG5. The two families of M. pyrsonotus segregating both sex determining loci are indicated by the pink circle containing a small blue square. Grey diamonds indicate the family was genotyped, but no associations were found with either LG5 or LG7. Open diamonds indicate genotyping was not performed, or that statistical association was not possible due to highly skewed sex ratios. The taxonomic relationships of the species are shown in the tree on the left.