Evolution of mir-92a Underlies Natural Morphological Variation in Drosophila melanogaster

Abstract

SummaryIdentifying the genetic mechanisms underlying phenotypic change is essential to understanding how gene regulatory networks and ultimately the genotype-to-phenotype map evolve. It is recognized that microRNAs (miRNAs) have the potential to facilitate evolutionary change [1–3]; however, there are no known examples of natural morphological variation caused by evolutionary changes in miRNA expression. Therefore, the contribution of miRNAs to evolutionary change remains unknown [1, 4]. Drosophila melanogaster subgroup species display a portion of trichome-free cuticle on the femur of the second leg called the “naked valley.” It was previously shown that Ultrabithorax (Ubx) is involved in naked valley variation between D. melanogaster and D. simulans [5, 6]. However, naked valley size also varies among populations of D. melanogaster, ranging from 1,000 up to 30,000 μm2. We investigated the genetic basis of intraspecific differences in the naked valley in D. melanogaster and found that neither Ubx nor shavenbaby (svb) [7, 8] contributes to this morphological difference. Instead, we show that changes in mir-92a expression underlie the evolution of naked valley size in D. melanogaster through repression of shavenoid (sha) [9]. Therefore, our results reveal a novel mechanism for morphological evolution and suggest that modulation of the expression of miRNAs potentially plays a prominent role in generating organismal diversity.

Systematic Study of Drosophila MicroRNA Functions Using a Collection of Targeted Knockout Mutations

“…miR-8 mutants showed leg and wing defects resulting from difficulties in eclosion from the pupal case (Karres et al, 2007). Differential expression of miR-92a in different strains of Drosophila correlates with the pattern of trichomes on the femur of the second leg, and miR-92a overexpression has been shown to lead to loss of trichomes (Arif et al, 2013). Consistent with this, Table 2.…”

A Perspective on Micro-Evo-Devo: Progress and Potential

“…Furthermore, it has been shown that changes in cis -regulatory sequences of svb and changes at the Ultrabithorax locus underlie the evolution of larval and leg trichome patterning, respectively, between species (Stern 1998; McGregor et al 2007). However, a recent study has shown that intraspecific variation in leg trichome patterns in Drosophila melanogaster is caused by changes in the expression of a microRNA, mir-92a (Arif et al 2013), which represses expression of shavenoid , a downstream target of svb (Schertel et al 2012; Arif et al 2013). The study by Arif and colleagues, therefore, not only revealed the genetic basis for morphological change, but also provided new insights into a well-characterized developmental GRN.…”

Evolution of flower color pattern through selection on regulatory small RNAs

“…The sequencing depth of the small RNA libraries was ~25M reads, with ~14M reads matching to the reference genome, full length, with no mis-matches or gaps allowed. The abundances of the reads were normalized using the reads per total method (22)(23)(24). The replicate to replicate differential expression was called on offset fold change, offset = 20 (empirically determined) (18,25) calculated on the proximal ends of maximal confidence intervals built on the available replicates.…”

“…Among the many documented cases of loci contributing to natural variation (22), several examples of small regulatory RNAs have been described (23)(24)(25)(26). However, these examples involve changes in expression pattern of pre-existing micro-RNAs or creation of new target sites, rather than de novo generation of a small regulatory RNA, as observed with SULF.…”