Divergent combinations of cis-regulatory elements control the evolution of phenotypic plasticity

Abstract

The widespread occurrence of phenotypic plasticity across all domains of life demonstrates its evolutionary significance. However, how plasticity itself evolves and how it contributes to evolution is poorly understood. Here, we investigate the predatory nematode Pristionchus pacificus with its feeding structure plasticity using recombinant-inbred-line and quantitative-trait-locus (QTL) analyses between natural isolates. We show that a single QTL at a core developmental gene controls the expression of the cannibalistic morph. This QTL is composed of several cis-regulatory elements. Through CRISPR/Cas-9 engineering, we identify copy number variation of potential transcription factor binding sites that interacts with a single intronic nucleotide polymorphism. Another intronic element eliminates gene expression altogether, mimicking knockouts of the locus. Comparisons of additional isolates further support the rapid evolution of these cis-regulatory elements. Finally, an independent QTL study reveals evidence for parallel evolution at the same locus. Thus, combinations of cis-regulatory elements shape plastic trait expression and control nematode cannibalism.

Conserved switch genes that arose via whole-genome duplication regulate a cannibalistic nematode morph

“…3A ) ( 19 ). A supergene locus plays a crucial role in P. pacificus mouth-form determination ( 20 , 21 ). Specifically, the eud-1/ sulfatase gene acts as a developmental switch, with eud-1 mutants constitutively St under all conditions ( 22 ).…”

Starvation resistance in the nematode Pristionchus pacificus requires a conserved supplementary nuclear receptor

“…Interestingly, this pattern is very different from the regulatory target patterns of its paralogs Ppa- NHR-1 and Ppa- NHR-40: most of their targets belong to the classes of metallopeptidases (astacins) and chitinases, which are crucial for cuticle degradation, and the vast majority of them are located on the X-chromosome [ 11 , 36 ]. This is the same chromosome that also harbors Ppa-nhr-1 and Ppa-nhr-40 , as well as the multi-gene locus that regulates the plastic switch decision [ 8 , 10 , 43 ]. This pattern, again, does not hold true for the loci harboring Ppa- NHR-10’s targets; it does not display a bias towards one particular chromosome, let alone chromosome X (Sup.…”

Genome evolution and divergence in cis-regulatory architecture is associated with condition-responsive development in horned dung beetles

“…In addition to coding sequence, epigenetic modifications such as histone marking are predicted to provide important mechanisms of plastic gene expression regulation (for reviews, see refs [4][5]). Further, recent quantitative trait locus (QTL) analysis combined with genome editing by CRISPR-Cas9 has begun to establish first causal connections between several cis-regulatory elements and the plastic development of nematode feeding structures [6]. Yet despite these advances, the genomic basis underlying developmental plasticity and its evolution, and in particular the role of the non-coding genome and chromatin architecture in regulating conditional responses in trait formation, remain largely unknown.…”