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crater lakes; divergent selection; geometric morphometrics; next-generation sequencing; RNA-Seq; sympatric speciation
Abstract:
The study of parallel evolution facilitates the discovery of common rules of diversification.
Here, we examine the repeated evolution of thick lips in Midas cichlid fishes (the
Amphilophus citrinellus species complex)—from two Great Lakes and two crater lakes
in Nicaragua—to assess whether similar changes in ecology, phenotypic trophic traits
and gene expression accompany parallel trait evolution. Using next-generation
sequencing technology, we characterize transcriptome-wide differential gene expression
in the lips of wild-caught sympatric thick- and thin-lipped cichlids from all four
instances of repeated thick-lip evolution. Six genes (apolipoprotein D, myelin-associated
glycoprotein precursor, four-and-a-half LIM domain protein 2, calpain-9, GTPase
IMAP family member 8-like and one hypothetical protein) are significantly underexpressed
in the thick-lipped morph across all four lakes. However, other aspects of lips’
gene expression in sympatric morphs differ in a lake-specific pattern, including the
magnitude of differentially expressed genes (97-510). Generally, fewer genes are differentially
expressed among morphs in the younger crater lakes than in those from the
older Great Lakes. Body shape, lower pharyngeal jaw size and shape, and stable
isotopes (d13C and d15N) differ between all sympatric morphs, with the greatest differentiation
in the Great Lake Nicaragua. Some ecological traits evolve in parallel (those
related to foraging ecology; e.g. lip size, body and head shape) but others, somewhat
surprisingly, do not (those related to diet and food processing; e.g. jaw size and shape,
stable isotopes). Taken together, this case of parallelism among thick- and thin-lipped
cichlids shows a mosaic pattern of parallel and nonparallel evolution.