Genetic basis and adaptive significance of yellow–blue colour variation in Lake Malawi cichlids

Supervisor: Dr Emília Santos

Co-Supervisor: George Turner

Project Summary (PhD):

Male nuptial colouration is among the most striking and rapidly diversifying traits in the East African cichlid radiations, where it is thought to play a central role in speciation by mediating mate choice and species recognition. Yet despite its importance, we still know remarkably little about the genetic architecture of colour divergence or whether repeated colour transitions arise through the same evolutionary mechanisms.

Yellow–blue male colour divergence has evolved repeatedly across the Lake Malawi radiation, distinguishing numerous closely related species. Selection on this trait appears to be strong, as almost all species are fixed for one or other colour phenotype. To uncover its genetic basis, we have established two independent QTL mapping crosses between yellow and blue species and are sequencing large F2 mapping populations to identify genomic regions controlling colour variation. In parallel, we have assembled a GWAS panel from the Lake Masoko population of Astatotilapia calliptera, an exceptional natural system in which yellow and blue males coexist within a single species, allowing us to identify loci underlying intraspecific variation. We have also recently identified three additional Lake Malawi populations that appear to harbour similar within-species colour polymorphisms. Sampling these populations will establish whether the polymorphism is heritable and variable within species, and provide material for comparative GWAS across multiple independent evolutionary origins. By integrating QTL mapping with comparative GWAS, we will determine whether repeated colour transitions are driven by shared genes, common developmental pathways, or entirely distinct genetic routes, providing a direct test of the predictability of adaptive evolution. Our established CRISPR/Cas9 toolkit for cichlid fishes enables rapid functional validation of the most promising candidate genes, allowing us to directly test the causal genetic basis of repeated colour evolution.

To establish the evolutionary significance of this variation, we will conduct mate-choice experiments to test for assortative mating between yellow and blue species. We will repeat these experiments under monochromatic lighting to test whether colour alone is sufficient to maintain reproductive isolation or whether additional sensory cues contribute to mate choice. Where feasible, we will run these same behavioural trials in polymorphic populations to determine whether assortative mating is already present before colour fixation, providing a rare opportunity to investigate the earliest stages of speciation in action. Investigation of F2 hybrids may be possible, allowing for preliminary investigations of whether colour and preference traits are strongly segregating and therefore have relatively simple genetic bases. These trials will involve behavioural observation, egg-collecting methods and/or molecular paternity testing of aquarium strains. 

Type of Work:

The student will investigate the genetic and behavioural basis of male colour variation and female preference in East African cichlid fishes. They will conduct fieldwork in Malawi and Tanzania to sample natural populations exhibiting colour variation, characterise their distribution, and establish the ecological context of this polymorphism. Aquarium trials will be conducted to assess the functional significance of colour variation and divergence in female preferences. They will generate and analyse genomic data from QTL crosses and wild populations using bioinformatic approaches to identify loci associated with colour divergence. The student will gain training in population genomics, quantitative genetics, CRISPR/Cas9 genome editing, fieldwork and mate choice experiments.

Importance of the area of research concerned:

Understanding how reproductive isolation evolves and contributes to speciation is a central goal in evolutionary biology. East African cichlid fishes provide an unparalleled opportunity to address this question, with repeated and rapid diversification of colour patterns across hundreds of species, implying a major role for sexually selected traits. However, we still lack a mechanistic understanding of how genetic changes generate novel phenotypes and reproductive barriers. By combining genomic mapping, functional validation, and mate choice experiments, this research will reveal whether repeated adaptive traits evolve through predictable genetic pathways, advancing our understanding of the origins of biodiversity.

References:

Divergent selection during speciation of Lake Malawi cichlid fishes inferred from parallel radiations in nuptial coloration https://www.pnas.org/doi/10.1073/pnas.2332665100 Genomic islands of speciation separate cichlid ecomorphs in an East African crater lake https://www.science.org/doi/10.1126/science.aac9927 Differential use of multiple genetic sex determination systems in divergent ecomorphs of an African crater lake cichlid https://www.biorxiv.org/content/10.1101/2021.08.05.455235v4 Female preference for conspecific males based on olfactory cues in a Lake Malawi cichlid fish https://royalsocietypublishing.org/doi/10.1098/rsbl.2005.0355.