Parsing parallel evolution: ecological divergence and differential gene expression in the adaptive radiations of thick‐lippedMidas cichlid fishes fromNicaragua

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

Genomics and the Evolution of Phenotypic Traits

“…Nonetheless, scans for functional differences can identify candidate genes that may harbor mutations involved in trait variation and adaptation (e.g., Hines et al 2012, Yang et al 2012, Coppe et al 2013). This can be particularly effective in parallel cases of phenotypic change (e.g., Jones et al 2012, Manousaki et al 2013.…”

Gene(s) and individual feeding behavior: Exploring eco‐evolutionary dynamics underlying left‐right asymmetry in the scale‐eating cichlid fishPerissodus microlepis

“…Similar or lower sample sizes had previously been successful in detecting feeding differences in other fish species (e.g., Ford et al., 2016; Kavembe et al., 2016; Manousaki et al., 2013) and the selection of the most extreme specimens contributes to maximize the power of finding differences between groups. The diet during the period over which a tissue is synthesized determines the stable isotope signatures of the tissue.…”

Molecular ecology studies of species radiations: current research gaps, opportunities and challenges

“…They address some of the most hotly debated evolutionary radiations in animals and plants, including cichlids (e.g. Schliewen et al 2001;Colombo et al 2013;Keller et al 2013;Manousaki et al 2013;Albertson et al 2014;Ford et al 2015), sticklebacks (Gow et al 2006;Berner et al 2010;Deagle et al 2013;Feulner et al 2013), Anolis lizards (Glor et al 2005;Ng & Glor 2011;Muñoz et al 2013), Heliconius butterflies (Nadeau et al 2013), Darwin 0 s finches (Petren et al 2005), plants of the Hawaiian silversword alliance (Lawton-Rauh et al 2007), oak trees (Cavender-Bares et al 2015) and bromeliads (Palma-Silva et al 2011). Due to the targeted nature of our search and the specific search terms used, our literature review is certainly not exhaustive.…”

“…Several studies achieved extensive sampling of nuclear genomes and transcriptomes using NGS approaches and compared the results to phenotypic diversity in radiating taxa, thus revealing mosaics of adaptive/parallel and neutral/nonparallel patterns of evolution (e.g. Keller et al 2013;Manousaki et al 2013;Nadeau et al 2013). Such mosaic patterns have long been predicted for ecological speciation and adaptive radiation in the face of gene flow (Gavrilets & Vose 2005;Nosil 2012).…”

“…Thus, we suspect that many researchers studying radiations will wish to turn to targeted resequencing as an attractive and feasible alternative to WGS. Transcriptome sequencing (RNA-seq) has also yielded valuable insights in studies of ecotype divergence, speciation and radiation (Nevado et al 2016), as also exemplified by two cichlid papers among the reviewed studies (Colombo et al 2013;Manousaki et al 2013). Nevertheless, due to the difficulty of sampling fresh material for proper RNA conservation and extraction, we suspect that future studies of radiations may wish to employ RNA-seq primarily as a marker discovery tool for subsequent exome (i.e.…”