Geography disentangles introgression from ancestral polymorphism in Lake Malawi cichlids

Abstract

Phenotypically diverse Lake Malawi cichlids exhibit similar genomes. The extensive sharing of genetic polymorphism among forms has both intrigued and frustrated biologists trying to understand the nature of diversity in this and other rapidly evolving systems. Shared polymorphism might result from hybridization and/or the retention of ancestrally polymorphic alleles. To examine these alternatives, we used new genomic tools to characterize genetic differentiation in widespread, geographically structured populations of Labeotropheus fuelleborni and Metriaclima zebra. These phenotypically distinct species share mitochondrial DNA (mtDNA) haplotypes and show greater mtDNA differentiation among localities than between species. However, Bayesian analysis of nuclear single nucleotide polymorphism (SNP) data revealed two distinct genetic clusters corresponding perfectly to morphologically diagnosed L. fuelleborni and M. zebra. This result is a function of the resolving power of the multi-locus dataset, not a conflict between nuclear and mitochondrial partitions. Locus-by-locus analysis showed that mtDNA differentiation between species (F(CT)) was nearly identical to the median single-locus SNP F(CT). Finally, we asked whether there is evidence for gene flow at sites of co-occurrence. We used simulations to generate a null distribution for the level of differentiation between co-occurring populations of L. fuelleborni and M. zebra expected if there was no hybridization. The null hypothesis was rejected for the SNP data; populations that co-occur at rock reef sites were slightly more similar than expected by chance, suggesting recent gene flow. The coupling of numerous independent markers with extensive geographic sampling and simulations utilized here provides a framework for assessing the prevalence of gene flow in recently diverged species.

Genetic interactions controlling sex and color establish the potential for sexual conflict in Lake Malawi cichlid fishes

“…LM rock-dwelling cichlids are ideal for investigating sex determination due to the existence of multiple sex systems not only between but also within species (Albertson, 2002;Streelman et al, 2003;Ser et al, 2010). The Malawi radiation has been so rapid that biological species continue to exchange genes by hybridization (for example, Mims et al (2010)) and major intrinsic post-zygotic incompatibilities separate only the most divergent lineages (Stelkens et al, 2010).…”

“…The rapidity of this radiation, extreme endemism (Parnell and Streelman, 2011) and continued low levels of gene flow between species (Mims et al, 2010) has led to a phenomenon wherein genetic incompatibilities between lineages are considerably outpaced by speciation (Stelkens et al, 2010). The integrity of species is maintained by pre-zygotic mechanismsassortative mating based on visual (Seehausen et al, 1997(Seehausen et al, , 2008van Oppen et al, 1998;Knight and Turner, 2004;Maan et al, 2004;Carleton, 2009), auditory (Amorim et al, 2004Simoes et al, 2008;Smith and van Staaden, 2009;Danley et al, 2011) and olfactory cues (Jordan et al, 2003;Plenderleith et al, 2005;Cole and Stacey, 2006) that sometimes breakdown.…”

“…The integrity of species is maintained by pre-zygotic mechanismsassortative mating based on visual (Seehausen et al, 1997(Seehausen et al, , 2008van Oppen et al, 1998;Knight and Turner, 2004;Maan et al, 2004;Carleton, 2009), auditory (Amorim et al, 2004Simoes et al, 2008;Smith and van Staaden, 2009;Danley et al, 2011) and olfactory cues (Jordan et al, 2003;Plenderleith et al, 2005;Cole and Stacey, 2006) that sometimes breakdown. Interspecific and intergeneric hybridization has been well documented within all of the African cichlid species flocks, including LM (Ruber et al, 2001;Salzburger et al, 2002;Smith and Kornfield, 2002;Smith et al, 2003;Streelman et al, 2004;Gerlai, 2007;Mims et al, 2010). Hybridization among such young species often produces viable, fertile offspring and maintains standing genetic and phenotypic variation (that is, the 'hybrid swarm' hypothesis, Seehausen, 2004;Genner and Turner, 2005;Loh et al, 2008;Parnell et al, 2008).…”

Do relaxed selection and habitat temperature facilitate biased mitogenomic introgression in a narrowly endemic fish?

“…2015), determining both the source species and factors structuring the introgression of hybrid genotypes could be difficult (Mims et al. 2010). In contrast, the substantial independent evolutionary history, metapopulation structure, and a minimal number of congeners in locations such as Cuatro Ciénegas could provide ideal systems to allow us to determine what are the major factors structuring introgression.…”

The macroecology of rapid evolutionary radiation

“…(a) Island biogeography and cichlid communities at broad scales Mbuna species exhibit high rates of endemism (53% of species were present at only one rock-reef site [26]), and extreme geographical structuring of population genetic variation [29,30,33,54]. At the broadest scales, we expected that (on average) species would co-occur less frequently than observed in random draws, not because they physically interact, but precisely because they do not.…”