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Etienne Danchin
Evolution & Diversité Biologique (UMR5174, EDB)

Genetic and nongenetic inheritance


Author(s): Danchin, E


Many biologists are calling for an ‘extended evolutionary synthesis’ that would ‘modernize the modern synthesis’ of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance and their interactions have important effects on evolutionary outcomes. I will define the terms of nongenetic inheritance and briefly review the evidence for such effects of epigenetic and cultural inheritance, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have major implications for diverse domains, including medicine where they may profoundly affect research strategies. For instance, non-genetic inheritance may explain a significant part of one of the major enigma of current molecular biology, namely missing heritability, which concerns many human supposedly genetic disorders. The missing heritability rather suggests that we should broaden our view of inheritance by including non-genetic inheritance into an inclusive theory of evolution.

Kevin Laland
University of St Andrews
School of Biology
United Kingdom

Genetic control of non-genetic inheritance: fact or fallacy?


Author(s): Laland, KN, Morgan, T, Fogarty, L, Mesoudi, A, Feldman, M, Smith, G


The foundation of the Modern Synthesis placed the gene at the centre of evolutionary explanations of biology, largely because at the time Mendelian genetics appeared to be the only general inheritance system. More recently, other non-genetic inheritance (henceforth NGI) systems (epigenetic inheritance, parental effects, ecological inheritance, social transmission and cultural inheritance) have been identified and been found to be widespread, raising questions about whether, and how, non-genetic inheritance might change the character of biological evolution. Here we draw on established empirical and theoretical findings from the cultural evolution, gene-culture coevolution, evolution of plasticity, and niche construction, literatures to illustrate ten ways in which non-genetic inheritance affects biological evolution. These include the findings that NGI systems can generate non-random (adaptive) variants; that they change the rate and dynamics of evolution, the pathways of information flow, and equilibria reached; that they alter the frequencies and spatial distribution of phenotypes; that they can propagate maladaptive variants; and that they change conceptions of fitness. These findings leave untenable the claims that non-genetic inheritance is under genetic control and as a consequence does not change the evolutionary process in biologically meaningful ways. Our analysis supports arguments for a broadening of current conceptions of biological evolution.

Angela Crean
University of New South Wales
School of Biological, Earth and Environmental Sciences

Like father like son? Nongenetic paternal effects reinvigorate the possibility of telegony


Author(s): Crean, AJ, Kopps, AM, Bonduriansky, R


Telegony, a belief that was once widely accepted but now largely dismissed, is the hypothesis that offspring occasionally inherit characters from a previous mate of their mother. Although telegony seems unfeasible under Mendelian laws of inheritance, mounting empirical evidence for nongenetic inheritance mechanisms reinvigorates the hypothesis. In the neriid fly, Telostylinus angusticollis, fathers transmit their environmentally-acquired condition to offspring: large fathers that are reared on a high-quality larval diet produce larger offspring. Males show no obvious forms of paternal investment or care, and thus the mechanism mediating the effect of paternal condition on offspring body size is not known. As a first step towards disentangling whether the effect is borne by the sperm itself or by accessory-gland products (ACPs) in the seminal fluid, we mated females initially to a male in high or low condition and then remated the female to a new male in high or low condition two weeks later. Interestingly, offspring size and viability were determined by the condition of the first male, with no effect of the condition of the second mate. Genetic tests confirm this result holds even when the second male is the biological father of the offspring. These findings suggest the paternal effect is mediated by ACPs, and provide a compelling case for reassessing the possibility of telegony as a valid phenomenon.

Marion East
Leibniz Institute for Zoo and Wildlife Research
Evolutionary Ecology

Maternal effects on offspring growth, survival and social status in spotted hyenas


Author(s): East, ML, Höner, OP, Wachter, B, Wilhelm, K, Burke, T, Hofer, H


We have studied two processes of non-genetic inheritance in a social mammal with linear dominance hierarchies. Firstly, in such species, the social status of an offspring at adulthood is often similar to the social position held by their mother; a phenomenon termed “rank inheritance”. Mothers may influence the rank obtained by their offspring at adulthood in at least three distinct ways: 1) the direct genetic inheritance of maternal traits that influence resource holding potential might predispose offspring to obtain a rank similar to that held by their mother, 2) the pre-natal maternal environment might influence offspring rank if foetal exposure to maternal androgens is related to maternal status and affects offspring competitiveness, and 3) maternal behavioural support, a component of the post-natal maternal environment, may help offspring to dominate those individuals that are subordinate to their mother, thereby assisting offspring to acquire a rank similar to that of their mother. We simultaneously test predictions derived from these three potential maternal effects on offspring rank acquisition at adulthood, using rare cases of offspring adoption detected by microsatellite profiling. We demonstrate that adopted offspring acquire a rank at adulthood similar to that of their surrogate mother and that the competitive ability of offspring at adulthood was best explained by post-natal maternal behavioural support. Secondly, we use long-term data to also show that high-born offspring have higher growth rates, are more likely to survive to adulthood and start reproduction at an earlier age than offspring of lower ranking mothers – thereby demonstrating a maternal ‘silver spoon effect’ in spotted hyenas.

Helene Collin
University of Liverpool
Ecology Evolution and Behaviour
United Kingdom

Non-genetic inheritance generated by exposure to anthropogenic stressors in the water flea (Daphnia pulex)


Author(s): Collin, H, Paterson, S, Plaistow, S


Understanding how populations rapidly adapt to anthropogenic change is imperative for predicting limits to population persistence and reducing species extinction rates. Since most random mutations decrease fitness, and even those that increase fitness initially only occur in a single individual in the population, it is hard to envisage how new mutations alone can explain rapid evolutionary responses. Rapid adaptation might arise through ‘soft selection’ operating on standing genetic variation. However, an emerging, alternative hypothesis that is that environment-induced non-genetic inheritance facilitates and speeds up adaptive evolution.
By decoupling phenotypic change from genotypic change, non-genetic inheritance (parental effects and epiallelic variation) is not subject to the limitations typically associated with genetic inheritance. However, our lack of understanding of the mechanism that underpin non-genetic inheritance, the transience and instability of non-genetically transmitted phenotypic states, and the way that non-genetic inheritance interacts with genetic inheritance, all greatly limit our ability to evaluate the significance non-genetic inheritance for long-term evolutionary change. We addressed this shortfall by performing a 4-generation experiment in which we exposed 3 clones of Daphnia pulex to sub-lethal doses of novel freshwater pollutants (heavy-metal, endocrine disruptor, herbicide) and then quantified the patterns of non-genetic inheritance generated over the next three generations. This was done at the individual trait level as well as at the multivariate level, using phenotypic trajectory analysis to quantify stressor-induced patterns of phenotypic integration over multiple generations. We evaluate whether non-genetic inheritance accumulates, persists or dissipates over multiple generations, whether these patterns differ for different types of stressor, and whether there is an interaction between genetic and non-genetic inheritance.

Jaime Grace
Uppsala University
Evolutionary Biology

Paternal effects on lifespan and aging in the fruit fly (Drosophila melanogaster)


Author(s): Grace, JL, Ryden, P, Friberg, U


Paternal effects are a potentially important source of non-genetic inheritance; however, attempts to quantify natural variation in paternal effects are often complicated by or confounded with maternal effects or the effects of genetic variation. Here we present a novel method for isolating and quantifying paternal effects using hemiclonal analysis. In Drosophila melanogaster, hemiclones have been used to replicate an entire haploid genome while holding the other haploid genome constant. We created hemiclones from diverse genetic backgrounds, including 38 inbred lines from the Drosophila Genome Reference Panel and 4 lines derived from other global populations. By crossing these hemiclones to homozygous females, we can select flies that are genetically identical, despite having fathers from genetically diverse backgrounds. We screen these 42 lines for variation in lifespan, a phenotype that harbors significant variation in the source populations, and is affected by a wide variety of genetic and non-genetic factors. Preliminary results indicate that there are significant differences in lifespan attributable to variation in paternal effects, and these results will further explore the relative importance of standing variation that exists within populations compared to the divergent variation that exists between populations. We will also consider the relative importance of paternal effects on early- vs late-stage mortality.

Julia Schroeder
Max Planck Institute for Ornithology

Sex specific social genetic effects in parental-care behaviour


Author(s): Schroeder, J, Dugdale, H, Burke, T, Nakagawa, S


The social environment, namely conspecifics, can influence the expression of phenotypes i.e., individuals other than the one expressing the trait in question can explain some of the phenotypic variation. The genetic part of this indirect effect represents an indirect genetic effect (IGE). Not accounting for IGEs can considerably under- or over-estimate the total heritable variation available for selection to act on, and thus predict misleading evolutionary trajectories. Yet, empirical studies on wild populations often ignore IGEs. We present a quantitative genetic analysis of biparental care in a wild, genetically pedigreed, bird population. Sex-specific IGEs increased the total heritable variation. Our data suggests that the female trait could evolve through indirect selection by her mating partner, which most theoretical models explaining the evolution of biparental care do not take into account. Notably, the within-individual repeatability of female parental care was lower than the total heritable variation. Our results show that the assumption that repeatability is the upper limit of heritability should be used cautiously when applying to socially interactive traits, and highlight the importance of accounting for social effects.

Rebecca Hoyle
University of Surrey
Department of Mathematics
United Kingdom

The fitness implications of adaptation via phenotypic plasticity and maternal effects


Author(s): Hoyle, RB, Ezard, THG, Prizak, R


In a changing environment, organisms face the challenge of using the most accurate environmental cues to construct phenotypes that optimise fitness. This environmentally specific phenotypic expression is delivered by phenotypic plasticity within the current generation and potentially also via previous generations through indirect or nongenetic inheritance.

Using a quantitative genetic model of adaptation via indirect genetic maternal effects, phenotypic plasticity and an additive genetic component, we show how the maternal effect coefficient that maximises population mean fitness depends on the predictability of environmental change (fast or slow, sinusoidal or stochastic) and the lag between development and selection. The impact of this developmental lag is particularly clear in rapidly changing stochastic environments.

We consider the influence on fitness of interactions between phenotypic plasticity and maternal effects. Expected mean population fitness is highest away from the peak levels of phenotypic plasticity, particularly in slowly or rarely changing environments. Phenotypic plasticity is highest when the lag between juvenile development and adult selection is shortest. We expect the relative influence of phenotypic plasticity and maternal effects to differ among environments, which may help to explain why we observe such a vast range of maternal effects coefficients empirically.

Sinead English
University of Oxford
Department of Zoology
United Kingdom

The information value of non-genetic inheritance in heterogeneous environments


Author(s): English, S, Shea, N, Pen, I, Uller, T


Parents contribute a variety of inputs to the development and fitness of their offspring beyond the transmission of DNA, including epigenetic marks, transfer of nutrients, antibodies and hormones, and behavioural interactions after birth. The evolutionary consequences of such non-genetic inheritance have been explored recently. By disconnecting what is selected from what is inherited, non-genetic inheritance can modify the course of evolution and selection on future generations. Less is known, however, about how mechanisms of non-genetic inheritance have themselves evolved. Here, we present a simple model to explore the adaptive evolution of non-genetic inheritance under different regimes of environmental change. Our model is based on a developmental switch that can evolve to produce different phenotypes in response to different levels of input. We consider genetic and non-genetic inputs as potential cues containing correlational information about coming selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. By exploring a range of temporal and spatial environmental fluctuation scenarios (cyclic and stochastic, of varying frequency), we evaluate the conditions that favour non-genetic inheritance as opposed to genetic determination of phenotype or within-generation plasticity. Finally, we use the model to exemplify three case studies which have provided hallmark examples of non-genetic inheritance: maternal effects on seed germination in plants, transgenerational phase shift in desert locusts and grandparental effects on dispersal polymorphisms in aphids.

Lára Hallsson
University of New South Wales
Evolution & Ecology Research Centre

The relative importance of genetic and nongenetic inheritance in relation to trait plasticity


Author(s): Hallsson, LR, Chenoweth, SF, Bonduriansky, R


A trait’s response to natural selection will reflect the nature of the inheritance mechanisms that mediate the transmission of variation across generations. The relative importance of genetic and nongenetic mechanisms of inheritance is predicted to be related to the degree of trait plasticity, with nongenetic inheritance playing a greater role in the cross-generational transmission of more plastic traits. However, this prediction has never been tested. We investigated the influence of genetic effects and nongenetic parental effects in two morphological traits differing in degree of plasticity by manipulating larval diet quality within a cross-generational split-brood experiment using the seed beetle Callososbuchus maculatus. In line with predictions, we found that the more plastic trait (elytron length) is strongly influenced by both maternal and paternal effects whereas genetic variance is undetectable. In contrast, the less plastic trait (first abdominal sternite length) is not influenced by parental effects but exhibits abundant genetic variance. Our findings support the hypothesis that environment-dependent parental effects may play a particularly important role in highly plastic traits and thereby affect the evolutionary response of such traits.


Chairman: Octávio S. Paulo
Tel: 00 351 217500614 direct
Tel: 00 351 217500000 ext22359
Fax: 00 351 217500028


XIV Congress of the European Society for Evolutionary Biology

Organization Team
Department of Animal Biology (DBA)
Faculty of Sciences of the University of Lisbon
P-1749-016 Lisbon


Computational Biology & Population Genomics Group