Department of Evolutionary Biology
A developmental switch gene for a feeding dimorphism in Pristionchus nematodes is coupled to micro- and macroevolution of plasticity
Author(s): Ragsdale, EJ, Müller, MR, Sommer, RJ
The mechanistic study of ecologically relevant traits is essential for understanding how ecology and development interact in the evolution of novel phenotypes. The nematode model Pristionchus pacificus shows plasticity in its teeth-like feeding structures, which are a novelty that enable predation of other nematodes. The plasticity consists of two discrete forms, stenostomatous (St) and eurystomatous (Eu), the latter bearing a claw-like dorsal tooth and an opposing subventral tooth. To study the genetic basis of the dimorphism, we used forward genetics to isolate Eu-form-defective (eud) mutants. A mutant with dominant alleles, eud-1, is haploinsufficient and was rescued by genetic transformation with a wild-type allele. Extra copies of this X-linked gene also drive highly St males to be Eu, indicating a role for EUD-1 in sexual dimorphism. Overexpression of eud-1 results in saturation of the Eu form and therefore acts as a dose-dependent master switch for the dimorphism. Further experiments revealed that EUD-1 is not only necessary and sufficient for the mouth-form decision in mutants but also represents a key determinant of micro- and macroevolutionary diversification. A survey of over 100 wild populations of P. pacificus gave a population genetics context, revealing natural variation in mouth-form phenotypes. Variation correlated with eud-1 expression, and genetic transformation of highly St strains confirmed the role of EUD-1 as a dimorphism switch. Thus, a gene identified by laboratory genetics can be a key player in natural history. Recent discovery of a sister species to P. pacificus, P. exspectatus, allows tests across species boundaries by the success of hybrid crosses, and transformation by this technique showed maintenance of the EUD-1 switch in macroevolution. By integrating genetics analysis, phylogenetics, and natural history, studies in this system ultimately aim to test the role of phenotypic plasticity in the evolution of novelty.
Dept of Ecological Sciences
A new perspective on phenotypic plasticity: taking into account physiological mechanisms challenges classic plasticity theory
Author(s): Ellers, J
Phenotypic plasticity is ubiquitous but we have poor knowledge about the underlying mechanisms. The reason for this is that classical studies of phenotypic plasticity developed and tested theory only for organismal traits, such as morphology or life history. However, a new and upcoming perspective on plasticity encompasses also transcriptional and physiological flexibility in an effort to study the underlying mechanisms of phenotypic plasticity. This raises the question how plasticity at different organisational levels interacts to produce the optimal phenotype in different environments. Here, I will focus on the evolution of temperature-induced plasticity as a case study to show that greater phenotypic plasticity at one organisational level is associated with environmental canalization (lack of plasticity) at the other level. More specifically, my work shows that strong physiological flexibility in response to temperature correlates with low sensitivity to temperature for fitness traits. In this context, I will discuss costs of plasticity and the evolution of plasticity as a means of adaptation to changing thermal conditions. I will also identify candidate physiological pathways underlying variation in thermal response. Ultimately, taking into account the mechanism underlying plasticity will challenge the classical dichotomy between phenotypic plasticity and environmental canalization. Instead, the key question is at what level of biological organization phenotypic plasticity will evolve.
Earth & Life Institute
Can we predict the effect of thermal fluctuations on specialist and generalist reaction norms?
Author(s): Foray, V, Desouhant, E, Gibert, P
Reaction norms depict the environmental effects on phenotypic traits and are used to predict the global change consequences on organisms. However, studies performed at constant temperatures have limited ecological significance because expressed phenotypes depend on the range and frequency of environmental states. By using the Jensen’s Inequality (a mathematical property of nonlinear functions), we predict that the effect of thermal fluctuations on the phenotype depends on the shape of the reaction norm: a negative effect of the thermal fluctuations when the reaction norm is convex and a positive effect when the reaction norm is concave. This study measures the impact of diel fluctuations in developmental temperature on phenotypic expression of traits related to fitness and energetic resources in two strains of the parasitoid wasp Venturia canescens differing in their thermal sensitivity. In a first experiment, we compare the effect of a constant versus a fluctuating thermal regime having the same means (20, 25 and 30 °C) on reaction norms of life history traits and of energetic reserves. In a second experiment, we examine the effects of a natural thermoperiod in field on these traits. As predicted, our results show that the shape of the reaction norm defines the phenotypic changes induced by the development under fluctuating thermal conditions. Moreover, our results emphasize the significance of taking into account several phenotypic life history traits to study the adaptive value of phenotypic plasticity. We also show that the level of energetic resources depends on the mean developmental temperature and not on the thermal regime. Finally, the field experiment confirms that the phenotype of these parasitoids depends on the temperature variation. This is the first experimental study demonstrating that Jensen’s Inequality can quantitatively predict the effect of thermal fluctuations on life-history traits of an ectotherm species.
Laboratoire des Sciences de l’Environnement Marin
Causes and consequences of developmental plasticity in Daphnia maturation
Author(s): Harney, ED, Van Dooren, TJM, Paterson, S, Plaistow, SJ
Maturation is a key life history transition, due to the importance of age and size at maturity in determining fitness. Understanding how maturation phenotypes evolve requires an appreciation of the underlying ontogenetic mechanisms, including the maturation threshold, which determines when an individual ‘decides’ to mature. Maturation thresholds are poorly understood, and little is known about how phenotypically plastic or genetically variable they are, but the parthenogenetic crustacean Daphnia is the ideal organism in which to study their evolution. Statistically modelling the maturation process shows that the maturation threshold is a developmentally plastic trait in response to variable resource availability, and more closely resembles a process with a rate than a discrete switch. The idea that the threshold is better thought of as a rate than a switch is further supported by gene expression changes during maturation. The maturation threshold also differs between genotypes and species of Daphnia, and clone-specific maternal effects in the development and growth rate interact to produce phenotypically plastic adult phenotypes. Furthermore, experiments studying the fitness consequences of maturation variation showed that Daphnia magna genotypes initiating maturation at smaller sizes had a higher intrinsic rate of population increase, but this size did not correlate well with competitive success when five clones were directly competed with each other, suggesting that interactions with other factors were influencing fitness. Maturation thresholds in Daphnia do not appear to be based on a single fixed state, but are responsive to environmental variation. The presence of heritable variation and transgenerational effects in these developmentally plastic traits suggests that they have an important role in the evolution of age and size at maturity.
Differential gene expression in a non-model fish species with alternative mating tactics
Author(s): Schunter, CM, Vollmer, S, Macpherson, E, Pascual, M
Social dominance is important for the reproductive success of males in many species. In fish with external fertilization, it is not as apparent which traits are necessary to become dominant or territorial and what benefits the socially dominant individual. In the black-faced blenny (Tripterygion delaisi) during the reproductive season, some males change color and invest in nest making and defense, whereas sneaker males do not change color and ‘sneak’ reproductions when females lay their eggs. Using RNAseq, we profiled differential gene expression between the brains of territorial males, sneaker males, and females to study the molecular signatures of male dimorphism. Despite several studies reporting high levels of genetic differentiation between sexes, we found that more genes were differentially expressed between the two male phenotypes than between males and females. This suggests that phenotypic plasticity is a more important factor in differential gene expression than sexual dimorphism during the reproductive period. For the dominant male, expression was higher in genes mainly related to cytoskeletal rearrangement indicating the drastic change in behavior and phenotype. We also identified novel genes which are differentially expressed in the brain tissue between the two male mating types in Tripterygion delaisi, which can be further investigated in other fish species with similar mating tactics.
Instituto de Ciencias Ambientales y Evolutivas
Discovering the genetic basis of torpor in a Chilean marsupial
Author(s): Cortes, PA, Bacigalupe, LL, Contreras, CCI, Varas, VV, Kemeid, VV, Blier, PPU, Opazo, JJC
Torpor is the physiologically controlled reduction of metabolic rate and body temperature experienced by small endotherms when facing periods of low temperature and/or food resources. This phenotype is characterized by an almost complete suppression of all expensive physiological processes with the aim of reducing energy expenditure. Nevertheless, some processes continue to operate at lower levels of activity, as they are critical for survival. The high demand of energy required during rewarming, to reach normothermy, represents an important constraint. Torpor and arousal from torpor involves a complex physiological reorganization at different organizational levels, underpinned by changes in genes expression. Accordingly in this study we investigated the reaction norm of (1) gene expression and (2) mitochondrial performance along different stages of torpor bout (deep torpor, arousal and normothermy) in the Chilean marsupial Thylamys elegans. More specifically we (1) performed a large-scale gene expression screening (RNA-seq) and (2) examined mitochondrial oxygen consumption and different enzymes of the electron transport system associated with torpor in liver. The gene expression profiles revealed a modest level of transcriptional changes along different stages of torpor bout. Functional analysis shows that genes involved in pathways associated to lipid metabolism are increased, whereas those involved in protein biosynthesis and detoxification are decreased during torpor and rewarming. For mitochondrial performance, high level of phenotypic flexibility was observed during the different stages of torpor. Taken together, these findings revealed important metabolic process those are critical during torpor in marsupials.
Institute of Plant Biology
Division of labour through phenotypic heterogeneity in clonal bacterial populations
Author(s): Kuemmerli, R, Schiessl, K, Bigosch, C, Ackermann, M
Individual bacteria in clonal populations often vary considerably in the expression of certain traits, even under uniform environmental conditions. At the proximate level, such phenotypic heterogeneity is generally attributed to stochastic processes that generate noise in gene expression. At the ultimate level, it remains often unclear whether phenotypic heterogeneity is beneficial and can be selected for. Here, we tested this possibility by studying between-individual variation in the production of a cooperative public good in the bacterium Pseudomonas aeruginosa. We show that phenotypic heterogeneity can provide benefits because it allows bacteria to realise an efficient form of division of labour. Specifically, we found that the production of public good followed an economy of scale: for the individual cell, the cost per public good molecule decreased with higher production rates. Accordingly, population-level costs of public good investment are minimized when only a fraction of the cells produces most of the public good, whilst benefits are equally shared among all individuals in the population. However, our data also indicate that the degree of division of labour is constrained by both the genetic architecture of the trait, and the overall need for the public good, which in turn depends on prevailing environmental conditions. Taken together, our data suggest a form of adaptive phenotypic plasticity, where individuals adjust their phenotype not only in response to environmental changes, but also in response to the population-level costs associated with the expression of a cooperative behaviour.
Centre for Functional and Evolutionary Ecologu=y
Evolution of discrete phenotypes from continuous norms of reaction
Author(s): Chevin, L, Lande, R
Discrete phenotypic variation often involves threshold expression of a trait with polygenic inheritance. How such discrete polyphenisms evolve starting from continuously varying phenotypes has received little theoretical attention. We model the evolution of sigmoid norms of reaction in response to variation in an underlying trait, or in a continuous environment, to identify conditions for the evolution of discontinuity. For traits with expression depending on a randomly varying underlying factor such as developmental noise, polyphenism is unstable under constant phenotypic selection for two selective peaks, and reaction norm evolution results in a phenotypic distribution concentrated at only one peak. But with frequency-dependent selection between two adaptive peaks, a steep threshold maintaining polyphenism generally evolves. For inducible plastic traits with expression conditioned on an environmental variable that also affects phenotypic selection, the steepness of the evolved reaction norm depends both on the differentiation of the environment in time or space, and on its predictability between development and selection, while bimodality of the environment has little effect per se. Together with recent measurements of genetic variance of threshold steepness, these predictions suggest that quasi-discrete phenotypic variation may often evolve from continuous norms of reactions, rather than being an intrinsic property of development.
Department of Zoology
Experimental evolution of plasticity in a virus
Author(s): Leggett, H, Buckling, A
Coinfection of parasite genotypes can select for various changes in parasite life history strategies, with consequences for disease dynamics and severity. Here we show adaptive phenotypic plasticity evolving in real time in response to coinfection under conditions in which both single infections and coinfections are common. We experimentally evolved an obligate-killing virus under conditions of single virus infections (single lines) or a mix of single infections and coinfections (mixed lines) and found mixed lines to evolve a plastic lysis time: they killed host cells more rapidly when coinfecting than when infecting alone. This behaviour resulted in high fitness under both infection conditions. We also discuss how population structure and the importance of within-patch prudence affects the fitness and virulence of populations of these viruses. Such plasticity and prudence has important consequences for the epidemiology of infectious diseases and the evolution of cooperation.
Department of Biological and Environmental Science
Fish farms select for increased phenotypic plasticity in growth and virulence in a fish pathogen
Author(s): Pulkkinen, K, Ketola, T, Laakso, J, Mappes, J, Sundberg, L
Opportunistic pathogens generally face two vastly different environments - within the host and outside host. One mechanism allowing for adaptation to alternating environments is switching between phenotypes (phenotypic plasticity). The opportunistic fish pathogen Flavobacterium columnare can be found from natural waters and from fish farms and it exhibits two reversible colony morphologies; a non-virulent “rough” and a virulent “rhizoid” morphology. As compared to natural waters, fish farms can be considered as extreme environments in terms of available host resources, but also in terms of stress caused by chemical and antibiotic treatments. Fish farms could thus be expected to impose higher selection pressures for coping between the within and outside host environment, and to select for increased phenotypic plasticity. To test these ideas we measured growth parameters of rhizoid and rough colony morphotypes of F. columnare isolates both from natural waters and from disease outbreaks at fish farms in different resource concentrations and temperatures, and tested their virulence with a zebrafish challenge model. We found that the non-virulent “rough” morphotypes had a higher growth rate and lower virulence than the “rhizoid” morphotypes, but only if the isolate was originating from the fish farms. This suggests that phenotypic plasticity between two morphotypes of opportunistic pathogen and their characteristic traits is clearly selected for in fish farms rather than in the natural environment.