A Developmental Switch Coupled to the Evolution of Plasticity Acts through a Sulfatase

Abstract

Developmental plasticity has been suggested to facilitate phenotypic diversity, but the molecular mechanisms underlying this relationship are little understood. We analyzed a feeding dimorphism in Pristionchus nematodes whereby one of two alternative adult mouth forms is executed after an irreversible developmental decision. By integrating developmental genetics with functional tests in phenotypically divergent populations and species, we identified a regulator of plasticity, eud-1, that acts in a developmental switch. eud-1 mutations eliminate one mouth form, whereas overexpression of eud-1 fixes it. EUD-1 is a sulfatase that acts dosage dependently, is necessary and sufficient to control the sexual dimorphism of feeding forms, and has a conserved function in Pristionchus evolution. It is epistatic to known signaling cascades and results from lineage-specific gene duplications. EUD-1 thus executes a developmental switch for morphological plasticity in the adult stage, showing that regulatory pathways can evolve by terminal addition of new genes.

Adaptive value of a predatory mouth-form in a dimorphic nematode

“…The presence of environmentally dependent fitness optima for the two forms suggests a fitness trade-off, satisfying the predicted conditions for the persistence of a discontinuous dimorphism in evolution [3]. The equilibrium of forms might expectedly change in populations as an adaptation to a particular host or microhabitat [41], and a diversity of ratios has indeed been observed in P. pacificus [7]. However, the persistence of conditions benefitting both forms would favour a dimorphism, provided that the cost of maintaining plasticity is not itself prohibitive [42].…”

“…In spite of mechanistic advances towards understanding the regulation and evolution of a developmental dimorphism in P. pacificus [7,19,25], the ecological context for morphological differences in this model organism was heretofore untested. Furthermore, the precise costs and benefits of resource polyphenisms under different environments have been generally difficult to determine in nature.…”

“…Predatory ability for each strain and mouth-form combination was assessed by the proportion of tested individuals able to successfully kill a prey item. Three strains of P. pacificus were assayed for predatory ability: (i) PS312, the laboratory reference strain ('California'); (ii) JU482 (Japan), which was previously noted to be a relatively successful predatory strain; and (iii) RS5205 (South Africa), which has a ratio of mouth-forms close to 1 : 1 in well-fed culture [7]. For each strain, 30 individuals of each mouth-form were assayed.…”

“…The Eu form is highly derived with respect to the closest outgroups that lack teeth, whereas the alternative, stenostomatous (St, 'narrow-mouthed') form is more reminiscent of outgroups in terms of mouth complexity and shape [9]. With such a dimorphism, this model system has been amenable to advances in understanding the genetic regulation of plasticity, including neuroendocrine signalling [19] and a developmental switch from a new gene [7].…”

“…Moreover, the majority of wild P. pacificus populations examined have a mouth-form frequency biased towards the Eu form (i.e. more than 50% of a population) when fed exclusively on bacteria [7], a diet that in nematodes requires neither teeth nor dimorphism. The production of both forms in every generation thus suggests a partial bethedging strategy that is based on probabilities for enhanced fitness under variable conditions [26].…”