MHC Adaptive Divergence between Closely Related and Sympatric African Cichlids

Abstract

BackgroundThe haplochromine cichlid species assemblages of Lake Malawi and Victoria represent some of the most important study systems in evolutionary biology. Identifying adaptive divergence between closely-related species can provide important insights into the processes that may have contributed to these spectacular radiations. Here, we studied a pair of sympatric Lake Malawi species, Pseudotropheus fainzilberi and P. emmiltos, whose reproductive isolation depends on olfactory communication. We tested the hypothesis that these species have undergone divergent selection at MHC class II genes, which are known to contribute to olfactory-based mate choice in other taxa.Methodology/Principal FindingsDivergent selection on functional alleles was inferred from the higher genetic divergence at putative antigen binding sites (ABS) amino acid sequences than at putatively neutrally evolving sites at intron 1, exon 2 synonymous sequences and exon 2 amino acid residues outside the putative ABS. In addition, sympatric populations of these fish species differed significantly in communities of eukaryotic parasites.Conclusions/SignificanceWe propose that local host-parasite coevolutionary dynamics may have driven adaptive divergence in MHC alleles, influencing odor-mediated mate choice and leading to reproductive isolation. These results provide the first evidence for a novel mechanism of adaptive speciation and the first evidence of adaptive divergence at the MHC in closely related African cichlid fishes.

Selection at the MHC class IIB locus across guppy (Poecilia reticulata) populations

“…These sites may also be involved in the affinity between the MHC and foreign antigens as amino acids that do not come into direct contact with the antigen can still affect binding through conformational changes (Foote and Winter, 1992). Positive selection in codons adjacent to the PBR has also been documented in the gila trout (Oncorhynchus gilae gilae; Peters and Turner, 2007), haplochromine cichlids (Pseudotropheus fainziberi and P. emmiltos; Blais et al, 2007) and in humans (Yang and Swanson, 2002).…”

“…However, recent advances in theory now make it feasible to detect differing dN/dS ratios across individual codons (Yang and Bielawski, 2000). These applications allow a more refined analysis to detect differing types of selection across the sequence itself (for example, Consuegra et al, 2005;Schaschl et al, 2005;Blais et al, 2007).…”

On the scent of speciation: the chemosensory system and its role in premating isolation

“…Conversely, although the most famous examples of speciation in fishes refer to visual cues (for example, three-spine sticklebacks: Rundle and Schluter, 1998; African cichlids: Seehausen and Alphen, 1998), olfaction also plays a significant role in speciation in some fish species. A recent example shows that adaptive divergence in MHC alleles influences odour-mediated mate choice and thus could have led to reproductive isolation among closely related African cichlid species (Blais, 2007). Chemical characterization of the signals involved in divergence allows the qualitative and quantitative comparison among blends emitted by different populations or species.…”

Parasite diversity, patterns of MHC II variation and olfactory based mate choice in diverging three-spined stickleback ecotypes

“…Among those mechanisms, habitat heterogeneity has only recently been the focus of research. A number of studies on MHC variation in neighboring populations proposed that habitat heterogeneity shapes MHC composition, probably due to contrasting parasites communities (Alcaide et al 2008;Babik et al 2008;Blais et al 2007;Ekblom et al 2007). …”