Genetic architecture of adaptive radiation across two trophic levels

Evolution of trophic diversity is a hallmark of adaptive radiation. Yet,
transitions between carnivory and herbivory are rare in young adaptive
radiations. Haplochromine cichlid fish of the African Great Lakes are
exceptional in this regard. Lake Victoria was colonized by an
insectivorous generalist and in less than 20,000 years, several clades of
specialized herbivores evolved. Carnivorous versus herbivorous lifestyles
in cichlids require many different adaptations in functional morphology,
physiology, and behaviour. Ecological transitions in either direction thus
require many traits to change in a concerted fashion, which could be
facilitated if genomic regions underlying these traits were physically
linked or pleiotropic. However, linkage/pleiotropy could also constrain
evolvability. To investigate components of the genetic architecture of a
suite of traits that distinguish invertivores from algae scrapers, we
performed Quantitative Trait Locus (QTL) mapping using a second-generation
hybrid cross. While we found indications of linkage/pleiotropy within
trait complexes, QTLs for distinct traits were distributed across several
unlinked genomic regions. Thus, a mixture of independently segregating
variation and some pleiotropy may underpin the rapid trophic transitions.
We argue that the emergence and maintenance of associations between the
different genomic regions underpinning co-adapted traits that evolved and
persist against some gene flow required reproductive isolation.