A histone demethylase links the loss of plasticity to nongenetic inheritance and morphological change

Abstract

Plasticity is a widespread feature of development, enabling phenotypic change based on the environment. Although the evolutionary loss of plasticity has been linked both theoretically and empirically to increased rates of phenotypic diversification, molecular insights into how this process might unfold are generally lacking. Here, we show that a regulator of nongenetic inheritance links evolutionary loss of plasticity in nature to changes in plasticity and morphology as selected in the laboratory. Across nematodes of Diplogastridae, which ancestrally had a polyphenism, or discrete plasticity, in their feeding morphology, we use molecular evolutionary analyses to screen for change associated with independent losses of plasticity. Having inferred a set of ancestrally polyphenism-biased genes from phylogenetically informed gene-knockouts and gene-expression comparisons, selection signatures associated with plasticity’s loss identify the histone H3K4 di/monodemethylase gene spr-5/LSD1/KDM1A. Manipulations of this gene affect both sensitivity and variation in plastic morphologies, and artificial selection of manipulated lines drive multigenerational shifts in these phenotypes. Our findings thus give mechanistic insight into how traits are modified as they traverse the continuum of greater to lesser environmental sensitivity.

Genetic regulators of a resource polyphenism interact to couple predatory morphology and behaviour

“…Another major insight of our study is that environmental conditions during development can cause a mismatch between morphology and behaviour. We found that an Eu-constitutive line exhibited the Eu morph across various environmental conditions that, in the wild-type, induce development of the St or Eu morph [37,50]. Strikingly, despite possessing Eu morphology, this strain exhibited St-like activity following development in St-inducing conditions.…”

“…Once cultures reached starvation conditions, as assessed by ~4-5 d without food and most adults having observably smaller body size than under well-fed conditions (between days 7 and 9 post-bleaching), individuals were assayed to assess the effect of starvation on predatory behaviour. Starvation prior to the adult stage, when the dimorphism is irreversibly expressed, induces a higher frequency of the Eu morph in wild-type strains [35,50], although its effects on constitutive mutants were previously unknown. Individuals reared in liquid culture were transferred to a 15 ml conical tube and centrifuged for 3 min at 1500 rpm 5 d post-bleaching.…”

“…Geometric morphometric data consisting of raw landmark coordinates for several strains, when reared under standard laboratory conditions, were obtained from a previous study [29]: the Eu-biased, laboratory reference strain PS312 for the wild-type Eu morph, mdt-15.1 mutants, nhr-1 loss-of-function mutants, nhr-40 loss-of-function mutants, mdt-15.1; nhr-1 double mutants and mdt-15.1; nhr-40 double mutants. Landmark data original to the present study, specifically of individuals of other strains reared under the same conditions as the above, were collected using previously produced images [50]: the St-biased isolate RS5200B for the wild-type St morph, and a line over-expressing eud-1, the integrated mutant rescue line eud-1 -; Ex[eud-1]. All samples used a previously defined set of 20 landmarks [29], and these data characterized the mouth shape, especially aspect ratio (width-to-height) and tooth shape, using both homologous and sliding landmarks.…”