The evolution of neurosensation drives the gain and loss of phenotypic plasticity

Phenotypic plasticity is widely regarded as important for enabling species resilience to environmental change and for species evolution. However, insight into the complex mechanisms by which phenotypic plasticity evolves in nature has been limited by our ability to reconstruct evolutionary histories of plasticity. By using part of the molecular mechanism, we were able to trace the evolution of pre-feeding phenotypic plasticity across the class Echinoidea and identify the origin of plasticity at the base of the regular urchins. The neurosensory foundation for plasticity was ancestral within the echinoids. However, coincident development of the plastic trait and the neurosensory system was not achieved until the regular urchins, likely due to pleiotropic effects and linkages between the two colocalized systems. Plasticity continues to evolve within the urchins with numerous instances of losses associated with loss of sensory capabilities and in one case loss of neurons, consistent with a cost associated with maintaining these capabilities. Thus, evidence was found for the neurosensory system providing opportunities and constraints to the evolution of phenotypic plasticity.

Prehatching Temperatures Drive Interannual Cohort Differences In Great Tit Metabolism

Basal metabolic rate (BMR) constitutes the lowest metabolic rate in a resting animal and is therefore considered to reflect the energetic cost of maintenance in endotherms. BMR is a reversible plastic trait that changes with environmental and ecological circumstances, albeit being heritable and susceptible to selection. Inter-individual variation within populations of small birds is substantial, and while many of the drivers of such variation have been identified, many remain unexplained. Some of the variation can be ascribed to cohort effects, indicating non-reversible developmental plasticity that will shape the adult metabolic phenotype. We studied winter BMR variation of juveniles over a fifteen-year period in a wild population of great tits Parus major at the northern border of their distribution. Here we show for the first time that winter BMR in cohorts of great tits changes among winters as a response to minimum ambient temperatures experienced early in life, during the prehatching period. This developmental plasticity might be adaptive if temperatures experienced by growing embryos would metabolically prime them to an environment that they will likely encounter in future life. However, in line with a more unpredictable future climate, the risk of phenotype-environment mismatch is likely to lead to certain cohorts being poorly adapted to prevailing winter conditions, resulting in wider annual fluctuations in population size.

Might Gene Duplication and Neofunctionalization Contribute to the Sexual Lability Observed in Fish?

Sex determination and differentiation varies widely across vertebrates, but is most dramatically diverse in fishes. Among fishes sex reversal and sex change are observed in 41 teleost families spanning 7 orders. These sex-changing fish perhaps highlight better than any other system that sex determination is not the narrow and fixed construct we once thought, but a plastic trait that is better viewed as a reaction norm. However, while this stunning transformation is increasingly understood, a fundamental question arises, which is why some fish species have retained this inherent plasticity in sexual fate, while others have not? Here, we explore our current understanding of sex change in fish, some of the factors that permit and constrain sex reversal, and posit that gene duplication and neofunctionalization contribute to the sexual lability observed in fish.

How kelp in drag lose their ruffles: Environmental cues, growth kinematics, and mechanical constraints govern curvature

We reveal how patterns of growth in response to environmental cues can produce curvature in biological structures by setting up mechanical stresses that cause elastic buckling.. Nereocystis luetkeana are nearshore kelp with wide ruffled blades that minimize self-shading in slow flow, but narrow flat blades that reduce hydrodynamic drag in rapid flow. Previously we showed blade ruffling is a plastic trait associated with a transverse gradient in longitudinal growth. Here we consider expansion and displacement of tissue elements due to growth in blades and find that growth patterns are altered by tensile stress due to hydrodynamic drag, but not by shading or nutrients. When longitudinal stress in a blade is low in slow flow, blade edges grow faster than midline in young tissue near the blade base. Tissue elements are displaced distally by expansion of younger proximal tissue. Strain energy caused by the transverse gradient in longitudinal growth is released by elastic buckling once the blade grows wide enough, producing ruffles distal to the region where the growth inhomogeneity started. If a blade experiences higher stress in rapid flow, edges and midline grow at the same rate, so the blade becomes flat as these new tissue elements are displaced distally.

Social aging: Late-life fitness gains explain the absence of a selection shadow in ants

A key hypothesis for the occurrence of senescence is a decrease in the selection strength because of low late-life fitness – the so-called selection shadow. However, in social insects, aging is considered a plastic trait and senescence seems to be absent. By life-long tracking of 102 ant colonies, we find that queens increase sexual productivity in late life regardless of their absolute lifespan or worker investment. This indicates a genetically accommodated adaptive shift towards increasingly queen-biased caste ratios over the course of a queens’ life. Furthermore, mortality decreased with age, supporting the hypothesis that aging is adaptive. We argue that selection for late life reproduction diminishes the selection shadow of old age and leads to the apparent absence of senescence in ants, in contrast to most iteroparous species.

A single-nucleotide change underlies the genetic assimilation of a plastic trait

Genetic assimilation—the evolutionary process by which an environmentally induced phenotype is made constitutive—represents a fundamental concept in evolutionary biology. Thought to reflect adaptive phenotypic plasticity, matricidal hatching in nematodes is triggered by maternal nutrient deprivation to allow for protection or resource provisioning of offspring. Here, we report natural Caenorhabditis elegans populations harboring genetic variants expressing a derived state of near-constitutive matricidal hatching. These variants exhibit a single amino acid change (V530L) in KCNL-1, a small-conductance calcium-activated potassium channel subunit. This gain-of-function mutation causes matricidal hatching by strongly reducing the sensitivity to environmental stimuli triggering egg-laying. We show that reestablishing the canonical KCNL-1 protein in matricidal isolates is sufficient to restore canonical egg-laying. While highly deleterious in constant food environments, KCNL-1 V530L is maintained under fluctuating resource availability. A single point mutation can therefore underlie the genetic assimilation—by either genetic drift or selection—of an ancestrally plastic trait.

A single nucleotide change underlies the genetic assimilation of a plastic trait

Genetic assimilation – the evolutionary process by which an ancestral environmentally sensitive phenotype is made constitutive – is a fundamental concept in biology. Its evolutionary relevance is debated, and our understanding of its prevalence, and underlying genetics and molecular mechanisms, is poor. Matricidal hatching is an extreme form of maternal provisioning induced by adverse conditions, which varies among Caenorhabditis elegans populations. We identified wild isolates, sampled from natural populations across multiple years and locations, that express a derived state of near-constitutive matricidal hatching. A single amino acid change in kcnl-1, encoding a small-conductance calcium-activated potassium channel subunit, explains most of this variation. A gain-of-function mutation altering the S6 transmembrane domain causes inappropriate activation of the K+ channel, leading to reduced vulval muscle excitability, and thus reduced expulsion of embryos, irrespective of environment. Using reciprocal allelic replacements, we show that this amino acid change is sufficient to induce constitutive matricidal hatching whilst re-establishing the ancestral protein abolishes matricidal hatching and restores egg-laying, thereby doubling lifetime reproductive fitness under benign conditions. While highly deleterious in the laboratory, experimental evolution showed that KNCL-1(V530L) is maintained under fluctuating resource availability. Selection on a single point mutation can therefore underlie the genetic assimilation of an ancestrally plastic trait with drastic life-history consequences.

A phenotypically plastic magic trait promoting reproductive isolation in sticklebacks?

This study identifies one possible mechanism whereby gene flow is interrupted in populations undergoing evolutionary divergence in sympatry; this is an important issue in evolutionary biology that remains poorly understood. Variation in trophic morphology was induced in three-spined stickleback by exposing them from an early age either to large benthic or to small pelagic prey. At sexual maturity, females given a choice between two breeding males, showed positive assortative mate choice for males raised on the same diet as themselves. The data indicate that this was mediated through a preference for males with trophic morphology similar to that of fish with which the females were familiar (from their pre-testing holding tanks). In trials where the female did not choose the most familiar male, the evidence suggests that either she had difficulty discriminating between two similar males or was positively choosing males with more extreme morphologies (more benthic-like or pelagic-like). This study has shown for the first time that expression of a plastic trait induced at an early age, not only results in specialisation for local foraging regimes but can also play a significant role in mate choice. This is equivalent to an environmentally induced, plastic version of the “magic traits” that promote ecologically-driven divergence in sympatry, hence the proposed descriptor “plastic magic trait”.