Foraging environment determines the genetic architecture and evolutionary potential of trophic morphology in cichlid fishes

Abstract

22Phenotypic plasticity allows organisms to change their phenotype in response to shifts in 23 the environment. While a central topic in current discussions of evolutionary potential, a 24 comprehensive understanding of the genetic underpinnings of plasticity is lacking in 25 systems undergoing adaptive diversification. Here we investigate the genetic basis of 26 phenotypic plasticity in a textbook adaptive radiation, Lake Malawi cichlid fishes. 27Specifically, we crossed two divergent species to generate an F 3 hybrid mapping 28 population. At early juvenile stages, hybrid families were split and reared in alternate 29 foraging environments that mimicked benthic/scraping or limnetic/sucking modes of 30 feeding. These alternate treatments produced variation in morphology that was broadly 31 2 similar to the major axis of divergence among Malawi cichlids, providing support for the 32 flexible stem theory of adaptive radiation. Next we found that the genetic architecture of 33 several morphological traits was highly sensitive to the environment. In particular, of 22 34 significant quantitative trait loci (QTL), only one was shared between environments. In 35 addition, we identified QTL acting across environments with alternate alleles being 36 differentially sensitive to the environment. Thus, our data suggest that while plasticity is 37 largely determined by loci specific to a given environment, it may also be influenced by 38 loci operating across environments. Finally, our mapping data provide evidence for the 39 evolution of plasticity via genetic assimilation at an important regulatory locus, ptch1. In 40 all, our data address longstanding discussions about the genetic basis and evolution of 41 plasticity. They also underscore the importance of the environment in affecting 42 developmental outcomes, genetic architectures, morphological diversity, and 43 evolutionary potential.

Adult plasticity in African cichlids: Rapid changes in opsin expression in response to environmental light differences

“…Along with opsin expression as depicted in the present study, plasticity acts across a broad range of cichlid phenotypes. These include trophic morphology (Muschick et al 2011), body shape (Wimberger 1992), gill and brain size in response to hypoxia (Crispo & Chapman 2010), foraging (Parsons et al 2016) and social behavior (Maruska & Fernald 2010). Plasticity allows an organism to quickly respond to an environmental shift instead of changing a phenotype through purely genetic means (mutation in the coding or regulatory sequences), which would simply be too slow.…”

Does phenotypic plasticity initiate developmental bias?

“…These induced responses have also been demonstrated as adaptive in that they can significantly improve foraging efficiency (Andersson, 2003;Day & McPhail, 1996;Parsons & Robinson, 2007). Notably, evidence suggests that these patterns of plasticity, particularly in the craniofacial region, are aligned with broader patterns of adaptive divergence in both cichlids and sticklebacks (Wund, Baker, Clancy, Golub, & Foster, 2008;Parsons et al, 2016;Wund, Valena, Wood, & Baker, 2012). The stickleback example is especially powerful as it demonstrates that populations of extant putative ancestors (i.e., marine sticklebacks) exhibit plastic responses with strong similarity to current benthic and limnetic ecotypes occurring repeatedly across independent lakes.…”

“…This is apparent across examples of adaptive radiation, population-level adaptive divergence or resource polymorphism, and in morphological plasticity. In (f,g), we see the outcome of plasticity experiments, with the effects of limnetic (long side) and benthic (short side) foraging treatments in F3 hybrid cichlids (from Parsons et al, 2016). Also, plasticity can show a similar pattern of response in spite of widely different environmental cues.…”

“…However, selection, as viewed by Darwin, does not specifically require genetic variation, rather it only needs variable fitness among phenotypes to operate and sort variation (Mayr, 1997). Indeed, among nongenetic sources of variation, a plethora of data now support the idea that environmentally induced phenotypes can provide variation for selection via phenotypic plasticity (Levis & Pfennig, 2016;Parsons, Sheets, Skúlason, & Ferguson, 2011;Parsons et al, 2016;Sultan, 2015). Thus, in Darwin's view, the source of variation for selection can be variable, and while he was naïve to genetic variation, it means variation that is generated outside a simple "genetic mutation-to-phenotypic-variant" process can contribute toward adaptative evolution.…”

Conservation Evo-Devo: Preserving Biodiversity by Understanding Its Origins

“…evo-devo on understanding how sources of variation arise has much to offer conservation 33 which focuses on preserving variation (i.e., biodiversity). This is because evo-devo has recently 34 become more applicable to population-level approaches through its maturing theoretical focus 35 and increased ability to account for continuous and complex phenotypic variation [15][16][17]. devo and conservation have the potential to form an important synergy, but what barriers to this 37 might remain?…”