Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects

RESEARCH ARTICLE Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects Snigdhadip Dey1, Stephen R. Proulx2*, Henrique Teotónio1* 1 Institut de Biologie de l´École Normale Supérieure, INSERM U1024, CNRS UMR 8197, Paris, France, 2 Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, Santa Barbara, California, United States of America * (SRP); (HT) Abstract OPEN ACCESS Citation: Dey S, Proulx SR, Teotónio H (2016) Adaptation to Temporally Fluctuating Environments by the Evolution of Maternal Effects. PLoS Biol 14(2): e1002388. doi:10.1371/journal.pbio.1002388 Academic Editor: Russell Bonduriansky, University of New South Wales, AUSTRALIA Received: December 17, 2015 Accepted: January 21, 2016 Published: February 24, 2016 Copyright: © 2016 Dey et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: Experimental design, data, and computer code are deposited at Dryad Digital Repository, openly available via http://dx.doi. org/10.5061/dryad.56bb4. Funding: This work received funding from the National Science Foundation (EF-1137835), the European Research Council (FP7/2007-286 2013/ 243285), and the "pepiniere interdisciplinaire" CNRSPSL Eco-Evo-Devo. All organisms live in temporally fluctuating environments. Theory predicts that the evolution of deterministic maternal effects (i.e., anticipatory maternal effects or transgenerational phenotypic plasticity) underlies adaptation to environments that fluctuate in a predictably alternating fashion over maternal-offspring generations. In contrast, randomizing maternal effects (i.e., diversifying and conservative bet-hedging), are expected to evolve in response to unpredictably fluctuating environments. Although maternal effects are common, evidence for their adaptive significance is equivocal since they can easily evolve as a correlated response to maternal selection and may or may not increase the future fitness of offspring. Using the hermaphroditic nematode Caenorhabditis elegans, we here show that the experimental evolution of maternal glycogen provisioning underlies adaptation to a fluctuating normoxia–anoxia hatching environment by increasing embryo survival under anoxia. In strictly alternating environments, we found that hermaphrodites evolved the ability to increase embryo glycogen provisioning when they experienced normoxia and to decrease embryo glycogen provisioning when they experienced anoxia. At odds with existing theory, however, populations facing irregularly fluctuating normoxia–anoxia hatching environments failed to evolve randomizing maternal effects. Instead, adaptation in these populations may have occurred through the evolution of fitness effects that percolate over multiple generations, as they maintained considerably high expected growth rates during experimental evolution despite evolving reduced fecundity and reduced embryo survival under one or two generations of anoxia. We develop theoretical models that explain why adaptation to a wide range of patterns of environmental fluctuations hinges on the existence of deterministic maternal effects, and that such deterministic maternal effects are more likely to contribute to adaptation than randomizing maternal effects. Competing Interests: The authors have declared that no competing interests exist. PLOS Biology | DOI:10.1371/journal.pbio.1002388 February 24, 2016 1 / 29 Adaptation and Maternal Effects Abbreviations: KR, Kenward-Roger; LMM, linear mixed-effect models; SNP, single-nucleotide polymorphism. Author Summary Mothers can influence the phenotype of their offspring, independently of the genes that they transmit to them; such phenomena are known as “maternal effects.” Theory suggests that maternal effects can be advantageous when the environment changes between generations, but a direct demonstration of this has been missing. Using the hermaphroditic nematode Caenorhabditis elegans, we show that the experimental evolution of maternal glycogen provisioning underlies the adaptation to a fluctuating normoxia–anoxia environment by increasing the survival of embryos under anoxic conditions. Evolution of this maternal effect only occurred in populations facing oxygen deprivation during embryogenesis every other generation (i.e., where fluctuation was regular or predictable). Unexpectedly, populations facing irregularly fluctuating oxygen levels did not evolve “bethedging” strategies, but instead adapted by the evolution of long-term transgenerational effects. Once evolved, maternal effects can nonetheless underlie adaptation to a wide range of temporally fluctuating environments. Introduction All organisms live in temporally fluctuating environments, for example, when the environmental conditions change regularly across seasons or when environmental conditions change erratically across a range of time spans. Adaptation to these environments can happen by the evolution of different degrees of within-generation phenotypic plasticity [1–3], as long as individuals have access to reliable information early in development, allowing them to forecast the environmental conditions they will experience later in their lives [4–7]. In many cases, however, the timing of development and environmental exposure does not coincide, making it unfeasible for individuals to independently acquire and use this sort of information [8,9], as when any portion of development occurs while individuals are still in the maternal environment and, therefore, the relevant information is only available through the mother. When environmental variation is negatively correlated between maternal and offspring generations, such as the seasonal weather changes that bivoltine insects may be faced with, selection can favor mothers that reliably cue their offspring to alter development and/or provision essential resources for offspring survival [5,10,11]. These maternal effects have been termed “anticipatory” maternal effects or transgenerational phenotypic plasticity [12–14]. Similarly, positively correlated environments, such as that of relatively constant and slowly fluctuating environments, can lead to the evolution of anticipatory maternal effects [5,15] and of a phenotypic “memory” of past environments [7,14,16–18]. In general, the rate of change in trait mean of a population because of selection equals its covariance with relative fitness [19,20]. In fluctuating environments, selection creates a positive covariance between the alleles individuals pass on to their progeny and the environment their mothers have experienced [21–23]. But because maternal effects may involve transfer of resources to offspring, within-generation developmental and physiological trade-offs can determine whether or not m (...truncated)