The gut microbiome is increasingly recognized for its impact on host fitness, but it remains poorly understood how naturally variable environments influence gut microbiome diversity and composition. ...We studied changes in the gut microbiome of ten genotypes of water fleas Daphnia magna in submerged mesocosm enclosures in a eutrophic lake over a period of 16 weeks, from early summer to autumn. The microbial diversity increased when Daphnia were reintroduced from the laboratory to the lake, and the composition of gut microbes drastically changed. Both gut microbiome diversity and composition continued to change over the 16‐week period, with alpha diversity peaking in late summer. The gut microbiome community was clearly distinct from that of the surrounding water, and temporal changes in the two communities were independent of each other. There were no consistent differences in the gut microbiomes among Daphnia genotypes in the lake environment. The change in gut microbiome over the season was accompanied by a decline in reproductive output and survival. There were weak, but statistically supported, effects of microbiota composition on Daphnia fitness, but there was no evidence that natural variation in microbiome diversity or composition was associated with tolerance to the cyanotoxin microcystin. We conclude that the gut microbiome of Daphnia is highly dynamic in a natural lake environment, but that host genetic effects on microbiome diversity and composition between genotypes within a population can be vanishingly small. These results emphasize that establishing the ecological effects of gut microbiota will require large‐scale experiments under natural conditions.
The evolution of female promiscuity poses an intriguing problem as benefits of mating with multiple males often have to arise via indirect, genetic, effects. Studies on birds have documented that ...multiple paternity is common in natural populations but strong evidence for selection via female benefits is lacking. In an attempt to evaluate the evidence more broadly, we review studies of multiple paternity in natural populations of all major groups of nonavian reptiles. Multiple paternity has been documented in all species investigated so far and commonly exists in over 50% of clutches, with particularly high levels in snakes and lizards. Marine turtles and lizards with prolonged pair‐bonding have relatively low levels of multiple paternity but levels are nevertheless higher than in many vertebrates with parental care. There is no evidence that high levels of polyandry are driven by direct benefits to females and the evidence that multiple paternity arises from indirect genetic benefits is weak. Instead, we argue that the most parsimonious explanation for patterns of multiple paternity is that it represents the combined effect of mate‐encounter frequency and conflict over mating rates between males and females driven by large male benefits and relatively small female costs, with only weak selection via indirect benefits. A crucial step for researchers is to move from correlative approaches to experimental tests of assumptions and predictions of theory under natural settings, using a combination of molecular techniques and behavioural observations.
The Mediterranean basin is a hotspot of biodiversity, fuelled by climatic oscillation and geological change over the past 20 million years. Wall lizards of the genus Podarcis are among the most ...abundant, diverse, and conspicuous Mediterranean fauna. Here, we unravel the remarkably entangled evolutionary history of wall lizards by sequencing genomes of 34 major lineages covering 26 species. We demonstrate an early (>11 MYA) separation into two clades centred on the Iberian and Balkan Peninsulas, and two clades of Mediterranean island endemics. Diversification within these clades was pronounced between 6.5-4.0 MYA, a period spanning the Messinian Salinity Crisis, during which the Mediterranean Sea nearly dried up before rapidly refilling. However, genetic exchange between lineages has been a pervasive feature throughout the entire history of wall lizards. This has resulted in a highly reticulated pattern of evolution across the group, characterised by mosaic genomes with major contributions from two or more parental taxa. These hybrid lineages gave rise to several of the extant species that are endemic to Mediterranean islands. The mosaic genomes of island endemics may have promoted their extraordinary adaptability and striking diversity in body size, shape and colouration, which have puzzled biologists for centuries.
Empirical studies of sexual traits continue to generate conflicting results, leading to a growing awareness that the current understanding of this topic is limited. Here we argue that this is because ...studies of sexual traits fail to encompass three important features of evolution. First, sexual traits evolve via natural selection of which sexual selection is just one part. Second, selection on sexual traits fluctuates in strength, direction and form due to spatial and temporal environmental heterogeneity. Third, phenotypic plasticity is ubiquitous and generates selection and responses to selection within and across generations. A move from purely gene-focused theories of sexual selection towards research that explicitly integrates development, ecology and evolution is necessary to break the stasis in research on sexual traits.
As is the case with any metaphor, parental effects mean different things to different biologists-from developmental induction of novel phenotypic variation to an evolved adaptation, and from ...epigenetic transference of essential developmental resources to a stage of inheritance and ecological succession. Such a diversity of perspectives illustrates the composite nature of parental effects that, depending on the stage of their expression and whether they are considered a pattern or a process, combine the elements of developmental induction, homeostasis, natural selection, epigenetic inheritance and historical persistence. Here, we suggest that by emphasizing the complexity of causes and influences in developmental systems and by making explicit the links between development, natural selection and inheritance, the study of parental effects enables deeper understanding of developmental dynamics of life cycles and provides a unique opportunity to explicitly integrate development and evolution. We highlight these perspectives by placing parental effects in a wider evolutionary framework and suggest that far from being only an evolved static outcome of natural selection, a distinct channel of transmission between parents and offspring, or a statistical abstraction, parental effects on development enable evolution by natural selection by reliably transferring developmental resources needed to reconstruct, maintain and modify genetically inherited components of the phenotype. The view of parental effects as an essential and dynamic part of an evolutionary continuum unifies mechanisms behind the origination, modification and historical persistence of organismal form and function, and thus brings us closer to a more realistic understanding of life's complexity and diversity.
Fifty years ago, Ernst Mayr published a hugely influential paper on the nature of causation in biology, in which he distinguished between proximate and ultimate causes. Mayr equated proximate ...causation with immediate factors (for example, physiology) and ultimate causation with evolutionary explanations (for example, natural selection). He argued that proximate and ultimate causes addressed different questions and were not alternatives. Mayr's account of causation remains widely accepted today, with both positive and negative ramifications. Several current debates in biology (for example, over evolution and development, niche construction, cooperation, and the evolution of language) are linked by a common axis of acceptance/rejection of Mayr's model of causation. We argue that Mayr's formulation has acted to stabilize the dominant evolutionary paradigm against change but may now hamper progress in the biological sciences.
The diversity of genetic and non-genetic processes that make offspring resemble their parents are increasingly well understood. In addition to genetic inheritance, parent-offspring similarity is ...affected by epigenetic, behavioural and cultural mechanisms that collectively can be referred to as non-genetic inheritance. Given the generality of the Price equation as a description of evolutionary change, is it not surprising that the Price equation has been adopted to model the evolutionary implications of non-genetic inheritance. In this paper, we briefly introduce the heredity perspectives on which those models rely, discuss the extent to which these perspectives make different assumptions and place different emphases on the roles of heredity and development in evolution, and the types of empirical research programmes they motivate. The existence of multiple perspectives and explanatory aims highlight, on the one hand, the versatility of the Price equation and, on the other hand, the importance of understanding how heredity and development can be conceptualized in evolutionary studies. This article is part of the theme issue 'Fifty years of the Price equation'.
Scientific activities take place within the structured sets of ideas and assumptions that define a field and its practices. The conceptual framework of evolutionary biology emerged with the Modern ...Synthesis in the early twentieth century and has since expanded into a highly successful research program to explore the processes of diversification and adaptation. Nonetheless, the ability of that framework satisfactorily to accommodate the rapid advances in developmental biology, genomics and ecology has been questioned. We review some of these arguments, focusing on literatures (evo-devo, developmental plasticity, inclusive inheritance and niche construction) whose implications for evolution can be interpreted in two ways—one that preserves the internal structure of contemporary evolutionary theory and one that points towards an alternative conceptual framework. The latter, which we label the ‘extended evolutionary synthesis' (EES), retains the fundaments of evolutionary theory, but differs in its emphasis on the role of constructive processes in development and evolution, and reciprocal portrayals of causation. In the EES, developmental processes, operating through developmental bias, inclusive inheritance and niche construction, share responsibility for the direction and rate of evolution, the origin of character variation and organism–environment complementarity. We spell out the structure, core assumptions and novel predictions of the EES, and show how it can be deployed to stimulate and advance research in those fields that study or use evolutionary biology.
The theoretical status of ‘niche construction’ in evolution is intensely debated. Here we substantiate the reasons for different interpretations. We consider two concepts of niche construction ...brought to bear on evolutionary theory; one that emphasizes how niche construction contributes to selection and another that emphasizes how it contributes to development and inheritance. We explain the rationale for claims that selective and developmental niche construction motivate conceptual change in evolutionary biology and the logic of those who reject these claims. Our analysis shows how the contention arises from alternative assumptions regarding the causal independence of the processes that generate variation, differential fitness and inheritance.
1. Introduction2. Selective Niche Construction
2.1. Selective niche construction interpreted as a challenge to the received view2.2. Selective niche construction interpreted as compatible with the received view2.3. A fault line in interpretative understanding3. Developmental Niche Construction
3.1. Developmental niche construction interpreted as a challenge to the received view3.2. Developmental niche construction interpreted as compatible with the received view3.3. A fault line in interpretative understanding4. Understanding the Fault Line
4.1. Causation in evolving systems5. Anomalies, Communication Failure, and Conceptual Change
Parents influence the development of their offspring in many ways beyond the transmission of DNA. This includes transfer of epigenetic states, nutrients, antibodies and hormones, and behavioural ...interactions after birth. While the evolutionary consequences of such non-genetic inheritance are increasingly well understood, less is known about how inheritance mechanisms evolve. Here, we present a simple but versatile model to explore the adaptive evolution of non-genetic inheritance. Our model is based on a switch mechanism that produces alternative phenotypes in response to different inputs, including genes and non-genetic factors transmitted from parents and the environment experienced during development. This framework shows how genetic and non-genetic inheritance mechanisms and environmental conditions can act as cues by carrying correlational information about future selective conditions. Differential use of these cues is manifested as different degrees of genetic, parental or environmental morph determination. We use this framework to evaluate the conditions favouring non-genetic inheritance, as opposed to genetic determination of phenotype or within-generation plasticity, by applying it to two putative examples of adaptive non-genetic inheritance: maternal effects on seed germination in plants and transgenerational phase shift in desert locusts. Our simulation models show how the adaptive value of non-genetic inheritance depends on its mechanism, the pace of environmental change, and life history characteristics.
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