When is a maternal effect adaptive
TL;DR: It is suggested that selection typically acts on maternal effects to maximise maternal rather than (or in addition to) offspring fitness, and many maternal effects will have an adaptive basis for mothers, regardless of whether these effects increase or decrease survival or reproductive success of individual offspring.
Abstract: Maternal effects have become an important field of study in evolutionary ecology and there is an ongoing debate regarding their adaptive significance. Some maternal effects can act to increase offspring fitness and are called 'adaptive maternal effects'. However, other maternal effects decrease offspring fitness and there is confusion regarding whether certain maternal effects are indeed adaptive or merely physiological inevitabilities. Here we suggest that the focus on the consequences of maternal effects for offspring fitness only and the use of 'snapshot' estimates of fitness have misdirected our effort to understand the evolution of maternal effects. We suggest that selection typically acts on maternal effects to maximise maternal rather than (or in addition to) offspring fitness. We highlight the importance of considering how maternal effects influence maternal fitness across a mother's lifetime and describe four broad types of maternal effects using an outcome-based approach. Overall, we suggest that many maternal effects will have an adaptive basis for mothers, regardless of whether these effects increase or decrease survival or reproductive success of individual offspring.
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TL;DR: The extent to which DOHaD represents the result of the physiological processes of developmental plasticity, which may have potential adverse consequences in terms of NCD risk later, or whether it is the manifestation of pathophysiological processes acting in early life but only becoming apparent as disease later?
Abstract: Extensive experimental animal studies and epidemiological observations have shown that environmental influences during early development affect the risk of later pathophysiological processes associated with chronic, especially noncommunicable, disease (NCD). This field is recognized as the developmental origins of health and disease (DOHaD). We discuss the extent to which DOHaD represents the result of the physiological processes of developmental plasticity, which may have potential adverse consequences in terms of NCD risk later, or whether it is the manifestation of pathophysiological processes acting in early life but only becoming apparent as disease later. We argue that the evidence suggests the former, through the operation of conditioning processes induced across the normal range of developmental environments, and we summarize current knowledge of the physiological processes involved. The adaptive pathway to later risk accords with current concepts in evolutionary developmental biology, especially those concerning parental effects. Outside the normal range, effects on development can result in nonadaptive processes, and we review their underlying mechanisms and consequences. New concepts concerning the underlying epigenetic and other mechanisms involved in both disruptive and nondisruptive pathways to disease are reviewed, including the evidence for transgenerational passage of risk from both maternal and paternal lines. These concepts have wider implications for understanding the causes and possible prevention of NCDs such as type 2 diabetes and cardiovascular disease, for broader social policy and for the increasing attention paid in public health to the lifecourse approach to NCD prevention.
891 citations
TL;DR: Recent studies of plants and animals show how studies of parental effects in an ecological context provide important insights into the origin and evolution of adaptation under variable environmental conditions.
Abstract: One of the outstanding challenges for evolutionary biologists is to understand how developmental plasticity can influence the evolutionary process. Developmental plasticity frequently involves parental effects, which might enable adaptive and context-dependent transgenerational transmission of phenotypic strategies. However, parent-offspring conflict will frequently result in parental effects that are suboptimal for parents, offspring or both. The fitness consequences of parental effects at evolutionary equilibrium will depend on how conflicts can be resolved by modifications of developmental processes, suggesting that proximate studies of development can inform ultimate questions. Furthermore, recent studies of plants and animals show how studies of parental effects in an ecological context provide important insights into the origin and evolution of adaptation under variable environmental conditions.
543 citations
TL;DR: This framework shows that, by decoupling phenotypic change from the genotype, nongenetic inheritance can circumvent the limitations of genetic inheritance and thereby influence population dynamics and alter the fitness landscape.
Abstract: Modern evolutionary biology is founded on the Mendelian-genetic model of inheritance, but it is now clear that this model is incomplete. Empirical evidence shows that environment (encompassing all external influences on the genome) can impose transgenerational effects and generate heritable variation for a broad array of traits in animals, plants, and other organisms. Such effects can be mediated by the transmission of epigenetic, cytoplasmic, somatic, nutritional, environmental, and behavioral variation. Building on the work of many authors, we outline a general framework for conceptualizing nongenetic inheritance and its evolutionary implications. This framework shows that, by decoupling phenotypic change from the genotype, nongenetic inheritance can circumvent the limitations of genetic inheritance and thereby influence population dynamics and alter the fitness landscape. The weight of theory and empirical evidence indicates that nongenetic inheritance is a potent factor in evolution that can engender ...
515 citations
Cites background from "When is a maternal effect adaptive"
...Nonetheless, there is considerable potential for parent-offspring conflicts over nongenetic inheritance (Lacey 1998, Marshall & Uller 2007, Uller 2008)....
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TL;DR: In resolving the conflict, distinctions should be drawn between PARs induced by normative variations in the developmental environment and the ill effects on development of extremes in environment such as a very poor or very rich nutritional environment.
Abstract: Many forms of developmental plasticity have been observed and these are usually beneficial to the organism The Predictive Adaptive Response (PAR) hypothesis refers to a form of developmental plasticity in which cues received in early life influence the development of a phenotype that is normally adapted to the environmental conditions of later life When the predicted and actual environments differ, the mismatch between the individual's phenotype and the conditions in which it finds itself can have adverse consequences for Darwinian fitness and, later, for health Numerous examples exist of the long-term effects of cues indicating a threatening environment affecting the subsequent phenotype of the individual organism Other examples consist of the long-term effects of variations in environment within a normal range, particularly in the individual's nutritional environment In mammals the cues to developing offspring are often provided by the mother's plane of nutrition, her body composition or stress levels This hypothetical effect in humans is thought to be important by some scientists and controversial by others In resolving the conflict, distinctions should be drawn between PARs induced by normative variations in the developmental environment and the ill effects on development of extremes in environment such as a very poor or very rich nutritional environment Tests to distinguish between different developmental processes impacting on adult characteristics are proposed Many of the mechanisms underlying developmental plasticity involve molecular epigenetic processes, and their elucidation in the context of PARs and more widely has implications for the revision of classical evolutionary theory
364 citations
Cites background from "When is a maternal effect adaptive"
...Indeed, in modelling conditions that might give rise to a PAR, Marshall & Uller (2007) found that the life-history characteristics of the trait were key determinants of the type of response that might be anticipated....
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TL;DR: Positive effect sizes found in this study are likely to be driven by a causal effect of egg size on offspring quality, but more studies that control for potential confounding effects of parental post‐hatching care, genes, and egg composition are needed to establish firmly this causal link.
Abstract: Parents affect offspring fitness by propagule size and quality, selection of oviposition site, quality of incubation, feeding of dependent young, and their defence against predators and parasites. Despite many case studies on each of these topics, this knowledge has not been rigorously integrated into individual parental care traits for any taxon. Consequently, we lack a comprehensive, quantitative assessment of how parental care modifies offspring phenotypes. This meta-analysis of 283 studies with 1805 correlations between egg size and offspring quality in birds is intended to fill this gap. The large sample size enabled testing of how the magnitude of the relationship between egg size and offspring quality depends on a number of variables. Egg size was positively related to nearly all studied offspring traits across all stages of the offspring life cycle. Not surprisingly, the relationship was strongest at hatching but persisted until the post-fledging stage. Morphological traits were the most closely related to egg size but significant relationships were also found with hatching success, chick survival, and growth rate. Non-significant effect sizes were found for egg fertility, chick immunity, behaviour, and life-history or sexual traits. Effect size did not depend on whether chicks were raised by their natural parents or were cross-fostered to other territories. Effect size did not depend on species-specific traits such as developmental mode, clutch size, and relative size of the egg, but was larger if tested in captive compared to wild populations and between rather than within broods. In sum, published studies support the view that egg size affects juvenile survival. There are very few studies that tested the relationship between egg size and the fecundity component of offspring fitness, and no studies on offspring survival as adults or on global fitness. More data are also needed for the relationships between egg size and offspring behavioural and physiological traits. It remains to be established whether the relationship between egg size and offspring performance depends on the quality of the offspring environment. Positive effect sizes found in this study are likely to be driven by a causal effect of egg size on offspring quality. However, more studies that control for potential confounding effects of parental post-hatching care, genes, and egg composition are needed to establish firmly this causal link.
362 citations
Cites background from "When is a maternal effect adaptive"
...This level was appropriate for their purpose since selection optimizes maternal, not offspring fitness (Marshall & Uller, 2007)....
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References
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Book•
01 Jan 1981
TL;DR: The genetic constitution of a population: Hardy-Weinberg equilibrium and changes in gene frequency: migration mutation, changes of variance, and heritability are studied.
Abstract: Part 1 Genetic constitution of a population: Hardy-Weinberg equilibrium. Part 2 Changes in gene frequency: migration mutation. Part 3 Small populations - changes in gene frequency under simplified conditions. Part 4 Small populations - less simplified conditions. Part 5 Small populations - pedigreed populations and close inbreeding. Part 6 Continuous variation. Part 7 Values and means. Part 8 Variance. Part 9 Resemblance between relatives. Part 10 Heritability. Part 11 Selection - the response and its prediction. Part 12 Selection - the results of experiments. Part 13 Selection - information from relatives. Part 14 Inbreeding and crossbreeding - changes of mean value. Part 15 Inbreeding and crossbreeding - changes of variance. Part 16 Inbreeding and crossbreeding - applications. Part 17 Scale. Part 18 Threshold characters. Part 19 Correlated characters. Part 20 Metric characters under natural selection.
20,288 citations
5,406 citations
"When is a maternal effect adaptive" refers background in this paper
...Whilst maternal effects were originally considered troublesome sources of variation in quantitative genetic studies (Falconer 1981), evolutionary ecologists now recognise maternal effects as one of the most important influences on offspring phenotype (Bernardo 1996a, Mousseau and Fox 1998, Wade 1998)....
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TL;DR: In this paper, the parent-offspring conflict in sexually reproducing species is viewed from the standpoint of the offspring as well as the parent, and it is shown that conflict is an expected feature of such relations.
Abstract: When parent-offspring relations in sexually reproducing species are viewed from the standpoint of the offspring as well as the parent, conflict is seen to be an expected feature of such relations. In particular, parent and offspring are expected to disagree over how long the period of parental investment should last, over the amount of parental investment that should be given, and over the altruistic and egoistic tendencies of the offspring as these tendencies affect other relatives. In addition, under certain conditions parents and offspring are expected to disagree over the preferred sex of the potential offspring. In general, parent-offspring conflict is expected to increase during the period of parental care, and offspring are expected to employ psychological weapons in order to compete with their parents. Detailed data on mother-offspring relations in mammals are consistent with the arguments presented. Conflict in some species, including the human species, is expected to extend to the adult reproductive role of the offspring: under certain conditions parents are expected to attempt to mold an offspring, against its better interests, into a permanent nonreproductive.
3,396 citations
"When is a maternal effect adaptive" refers background in this paper
...…both, selection will typically maximise maternal, rather than offspring fitness, particularly in species with no post-natal maternal care where the evolution of offspring counter-strategies may be less likely to evolve (Smith and Fretwell 1974, Trivers 1974, Bernardo 1996a, Marshall et al. 2006)....
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TL;DR: The relationship between the energy expended per offspring, fitness of offspring, and parental fitness is presented in a two-dimensional graphical model and the validity of the model in determining an optimal parental strategy is demonstrated analytically.
Abstract: The relationship between the energy expended per offspring, fitness of offspring, and parental fitness is presented in a two-dimensional graphical model. The validity of the model in determining an optimal parental strategy is demonstrated analytically. The model applies under various conditions of parental care and sibling care for the offspring but is most useful for species that produce numerous small offspring which are given no parental care.
2,780 citations
"When is a maternal effect adaptive" refers background in this paper
...…both, selection will typically maximise maternal, rather than offspring fitness, particularly in species with no post-natal maternal care where the evolution of offspring counter-strategies may be less likely to evolve (Smith and Fretwell 1974, Trivers 1974, Bernardo 1996a, Marshall et al. 2006)....
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...For example, increasing average propagule size incurs a fecundity cost in either the immediate or subsequent rounds of reproduction (Smith and Fretwell 1974)....
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TL;DR: The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity.
Abstract: The costs and limits of phenotypic plasticity are thought to have important ecological and evolutionary consequences, yet they are not as well understood as the benefits of plasticity. At least nine ideas exist regarding how plasticity may be costly or limited, but these have rarely been discussed together. The most commonly discussed cost is that of maintaining the sensory and regulatory machinery needed for plasticity, which may require energy and material expenses. A frequently considered limit to the benefit of plasticity is that the environmental cues guiding plastic development can be unreliable. Such costs and limits have recently been included in theoretical models and, perhaps more importantly, relevant empirical studies now have emerged. Despite the current interest in costs and limits of plasticity, several lines of reasoning suggest that they might be difficult to demonstrate.
2,109 citations