Sexual conflict resolved by invasion of a novel sex determiner in Lake Malawi cichlid fishes

Abstract

Sex determination mechanisms differ among animal species, but it is not clear how these differences evolve. New sex determiners may arise in response to sexual conflicts, which occur when traits benefit one sex but hinder the other. We identified the genetic basis for the orange-blotch (OB) color pattern, a trait under sexually antagonistic selection in the cichlid fish of Lake Malawi, East Africa. The OB phenotype is due to a cis-regulatory mutation in the Pax7 gene. OB provides benefits of camouflage to females but disrupts the species-specific male color patterns used for mate recognition. We suggest that the resulting sexual conflict over the OB allele has been resolved by selection for a novel female sex determination locus that has invaded populations with an ancestral male sex determination system.

Figure 1

OB pigmentation affects different aspects of fitness in females and males. (A) Typical female BB (top) and OB (bottom) morphs, represented by Tropheops ‘orange chest’. (B) Common BB male nuptial coloration (top) and rare OB male (bottom) of Labeotropheus fuelleborni. (C) OB (white arrow) and BB (black arrow) L. fuelleborni females are differently cryptic over the boulder reef habitat at Nankoma Island (13°53′30″S, 34°36′43″E; frame from Movie S1).

Figure 2

Genetic mapping in families and natural populations. (A) Individual recombinant chromosomes (rows) at the OB locus from pedigreed families, with “OB” and “BB” indicating genotypes of inherited maternal alleles, and empty blocks indicating non-informative markers. Marker names and Mb position on Tetraodon Chr.11 are indicated at top of marker columns. Breakpoint analysis across multiple recombinants defines an OB interval between markers AKR7A2 and SKI; one recombinant refines the interval to AKR7A2 and MET4802. Italics indicate gene-associated markers. (B) Collecting sites in Lake Malawi. The populations analyzed in panels C-G are marked with orange stars (c-g). Localities combined for the lake-wide mapping panel (H) are marked with red dots. (C-G) Association of markers with OB and OB-like phenotypes in populations, graphed as LOD of association versus position on Tetraodon Chr.11. (C) M. zebra Makonde (24 BB, 24 WhB & Wh); (D) M. zebra ‘blaze’ Manda (24 BB, 16 OB & O); (E) M. xanstomachus Nankoma (26 BB, 22 OB); (F) L. trewavasae Thumbi West (24 BB, 24 OB & O); (G) Tropheops ‘orange chest’ Thumbi West (32 BB, 18 OB). (H) Multi-species lake-wide mapping panel (34 BB, 44 OB class; Table S2).

Figure 3

Pax7 expression is increased in OB individuals independent of species and morph. (A) Pax7 expression relative to BB expression level within each species, measured by quantitative real-time PCR of juvenile tailfin RNA and normalized to β-actin expression. OB genotypes and expressed phenotypes are indicated along the x-axis. (B, C) Allele-specific expression using RT-PCR of a size polymorphism in the 5′UTR of Pax7. (B) Representative size separation traces of products from +/+ and OB/+ individuals, with allele type and size indicated above peaks. (C) The ratio of OB- to non-OB-sized allele expression. All p values from pairwise t-tests.