The genetic basis of coordinated plasticity across functional units in a Lake Malawi cichlid mapping population

Abstract

Adaptive radiations are often stereotypical, as populations repeatedly specialize along conserved environmental axes. Phenotypic plasticity may be similarly stereotypical, as individuals respond to environmental cues. These parallel patterns of variation, which are often consistent across traits, have led researchers to propose that plasticity can facilitate predictable patterns of evolution along environmental gradients. This "flexible stem" model of evolution raises questions about the genetic nature of plasticity, including how complex is the genetic basis for plasticity? Is plasticity across traits mediated by many distinct loci, or few "global" regulators? To address these questions, we reared a hybrid cichlid mapping population on alternate diet regimes mimicking an important environmental axis. We show that plasticity across an array of ecologically relevant traits is generally morphologically integrated, such that traits respond in a coordinated manner, especially those with overlapping function. Our genetic data are more ambiguous. While our mapping experiment provides little evidence for global genetic regulators of plasticity, these data do contain a genetic signal for the integration of plasticity across traits. Overall, our data suggest a compromise between genetic modularity, whereby plasticity may evolve independently across traits, and low level but widespread genetic integration, establishing the potential for plasticity to experience coordinated evolution.

The transcriptional state and chromatin landscape of cichlid jaw shape variation across species and environments

“…A number of general themes emerge from these data. First, they provide clear support for the hypothesis that foraging environment influences the genotype-phenotype map for craniofacial skeletal traits (Parsons et al, 2016;Navon et al, 2021;Zogbaum et al, 2021). More specifically, our data suggest that pelagic foraging "drives" species-and environment-specific DE.…”

“…In particular, to address the question of genetic and epigenetic control of plasticity in the cichlid feeding apparatus, we utilize two complementary methods of assessing transcriptional output: RNA-seq to analyze gene expression, and ATAC-seq to assess chromatin accessibility. We focused on an important functional complex -i.e., the interopercle-retroarticular (IOP-RA) complex -which (1) is part of the opercle 4-bar linkage chain, (2) helps to drive lower jaw depression, (3) is comprised of hard and soft tissues, (4) varies among Malawi cichlids in a manner that predicts foraging mode/habitat, and (5) has been shown to be plastic in previous research (Figure 1; Hu and Albertson 2014;Navon et al 2021). Our goals are to identify genes that are both differentially expressed (DE) and differentially accessible (DA) between species and environments.…”

The transcriptional state and chromatin landscape of cichlid jaw shape variation across species and environments

“…A number of general themes emerge from these data. First, they provide further support for the hypothesis that foraging environment influences the genotype-phenotype map for craniofacial skeletal traits (Navon et al, 2021;Parsons et al, 2016;Zogbaum et al, 2021). More specifically, our data suggest that pelagic foraging is an especially potent driver of species-and environment-specific differential gene expression.…”

“…We utilize two complementary methods of assessing transcriptional output: RNA-seq to analyse gene expression and ATAC-seq to assess chromatin accessibility. We focus on an important functional complex-that is, the interopercleretroarticular (IOP-RA) linkage-which (1) is part of the opercle 4bar system, (2) helps to drive lower jaw depression, (3) is comprised of hard and soft tissues, (4) varies among Malawi cichlids in a manner that predicts foraging mode/habitat, and (5) has been shown to be plastic in previous research (Figure 1; Hu & Albertson, 2014, 2017Navon et al, 2021). Environmental input is explicitly incorporated into our experimental design, as we force animals to collect prey in a manner that mimics alternate benthic-pelagic modes of feeding.…”

Qualified agreement: How scientific discoveries support theistic belief

“…The two groups developed into adults with distinctly different head-jaw structures that were tailored to forage for the available food most effectively. Navon et al reported on a similar experiment that confirmed the Parsons et al results (Navon et al 2021). The investigators also demonstrated diet-induced adaptive changes to body shape and fin-ray number.…”