The human-microbial ecosystem plays a variety of important roles in human health and disease. Each person can be viewed as an island-like “patch” of habitat occupied by microbial assemblages formed by the fundamental processes of community ecology: dispersal, local diversification, environmental selection, and ecological drift. Community assembly theory, and metacommunity theory in particular, provides a framework for understanding the ecological dynamics of the human microbiome, such as compositional variability within and between hosts. We explore three core scenarios of human microbiome assembly: development in infants, representing assembly in previously unoccupied habitats; recovery from antibiotics, representing assembly after disturbance; and invasion by pathogens, representing assembly in the context of invasive species. Judicious application of ecological theory may lead to improved strategies for restoring and maintaining the microbiota and the crucial health-associated ecosystem services that it provides.

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The Application of Ecological Theory Toward an Understanding of the Human Microbiome

The underwater environment is filled with biotic and abiotic sounds, many of which can be important for the survival and reproduction of fish. Over the last century, human activities in and near the water have increasingly added artificial sounds to this environment. Very loud sounds of relatively short exposure, such as those produced during pile driving, can harm nearby fish. However, more moderate underwater noises of longer duration, such as those produced by vessels, could potentially impact much larger areas, and involve much larger numbers of fish. Here we call attention to the urgent need to study the role of sound in the lives of fish and to develop a better understanding of the ecological impact of anthropogenic noise.

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A noisy spring: the impact of globally rising underwater sound levels on fish

Sympatric speciation, the evolution of reproductive isolation without geographic barriers, remains highly contentious. As a result of new empirical examples and theory, it is now generally accepted that sympatric speciation has occurred in at least a few instances, and is theoretically plausible. Instead, debate has shifted to whether sympatric speciation is common, and whether models’ assumptions are generally met in nature. The relative frequency of sympatric speciation will be difficult to resolve, because biogeographic changes have obscured geographical patterns underlying many past speciation events. In contrast, progress is being made on evaluating the empirical validity of key theoretical conditions for sympatric speciation. Disruptive selection and direct selection on mating traits, which should facilitate sympatric speciation, are biologically well supported. Conversely, costs to assortative mating are also widely documented, but inhibit speciation. Evaluating the joint incidence of these key fac...

Sympatric Speciation: Models and Empirical Evidence

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 the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, 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 implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.

Beyond DNA: integrating inclusive inheritance into an extended theory of evolution

Speciation with gene flow is greatly facilitated when traits subject to divergent selection also contribute to non-random mating. Such traits have been called ‘magic traits’, which could be interpreted to imply that they are rare, special, or unrealistic. Here, we question this assumption by illustrating that magic traits can be produced by a variety of mechanisms, including ones in which reproductive isolation arises as an automatic by-product of adaptive divergence. We also draw upon the theoretical literature to explore whether magic traits have a unique role in speciation or can be mimicked in their effects by physically linked trait-complexes. We conclude that magic traits are more frequent than previously perceived, but further work is needed to clarify their importance.

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Magic traits in speciation: 'magic' but not rare?

Learning is widespread in nature, occurring in most animal taxa and in several different ecological contexts and, thus, might play a key role in evolutionary processes. Here, we review the accumulating empirical evidence for the involvement of learning in mate choice and the consequences for sexual selection and reproductive isolation. We distinguish two broad categories: learned mate preferences and learned traits under mate selection (such as bird song). We point out that the context of learning, namely how and when learning takes place, often makes a crucial difference to the predicted evolutionary outcome. Factors causing biases in learning and when one should expect the evolution of learning itself are also explored.

The impact of learning on sexual selection and speciation.

The Lake Victoria ‘species flock’ of cichlids is puzzling because reproductive isolation often occurs in the absence of substantial ecological differences among species. Theory predicts that this cannot evolve with most genetic mechanisms for mate choice. We provide the first evidence that learning, in the form of sexual imprinting, helps maintain reproductive isolation among closely related cichlid species. Using a cross-fostering experiment, we show that young females develop a sexual preference for males of their foster mothers' species, even reversing species assortative mating preferences. We suggest that learning creates favourable conditions for reproductive isolation to evolve.

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Early learning influences species assortative mating preferences in Lake Victoria cichlid fish.

Sound plays an important role in the life of many animals, including many bird species. Typically, male birds sing to defend a territory and to attract mates. Ambient noise may negatively affect the signal efficiency of their songs, which may be critical to reproductive success. Consequently, anthropogenic noise may be detrimental to individual birds and to populations in cities and along highways. Several bird species that are still common in urban areas have been shown to sing at higher frequency at locations where there is more low-frequency traffic noise. Here we show that chiffchaffs along noisy highways also sing with a higher minimum frequency than chiffchaffs nearby at a quiet riverside. Furthermore, through experimental exposure to highway noise we show that these birds are capable of making such adjustments over a very short time scale. The first 10 songs sung during the noise exposure revealed an immediate shift to higher frequencies, with a return to pre-exposure levels in recordings without noise the following day. In a transmission re-recording experiment we tested the impact of a potential measurement artifact by recording playback of the same songs repeatedly under different controlled noise conditions. We found an upward shift in the minimum frequency measurement associated with more noisy recordings of the same song, but this artifact was not of a scale that it could explain the noise-dependent spectral shifts in chiffchaffs.

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Immediate spectral flexibility in singing chiffchaffs during experimental exposure to highway noise

Many models have investigated how the process of speciation may occur in sympatry. In these models, individuals are either asexual or mate choice is determined by very simple rules. Females, for example, may be assumed either to compare their phenotype to that of a potential mate, preferring to mate with similar males (phenotype matching), or to possess preference genes that determine which male phenotype they prefer. These rules often do not reflect the mate-choice rules found in empirical studies. In this paper, we compare these two modes of female choice with various types of sexual imprinting. We examine the efficacy of different mate-choice behavior in causing divergence in male traits under simple deterministic one-locus population genetic models as well as under polygenic, individual-based simulations based on the models of Dieckmann and Doebeli (1999). We find that the inheritance mechanism of mate choice can have a large effect on the ease of sympatric speciation. When females imprint on their mothers, the result of the model is similar to phenotype matching, where speciation can occur fairly easily. When females imprint on their fathers or imprint obliquely, speciation becomes considerably less likely. Finally, when females rely on preference genes, male trait evolution occurs easily, but the correlation between trait and preference can be weak, and interpreting these results as speciation may be suspect.

Machteld N. Verzijden

Papers

The impact of learning on sexual selection and speciation.

Early learning influences species assortative mating preferences in Lake Victoria cichlid fish.

Immediate spectral flexibility in singing chiffchaffs during experimental exposure to highway noise

Female mate-choice behavior and sympatric speciation.

Sexual imprinting can induce sexual preferences for exaggerated parental traits.