Timothée Bonnet

Hybrid speciation in sparrows II: a role for sex chromosomes?

Homoploid hybrid speciation in animals is poorly understood, mainly because of the scarcity of well‐documented cases. Here, we present the results of a multilocus sequence analysis on the house sparrow (Passer domesticus), Spanish sparrow (P. hispaniolensis) and their proposed hybrid descendant, the Italian sparrow (P. italiae). The Italian sparrow is shown to be genetically intermediate between the house sparrow and Spanish sparrow, exhibiting genealogical discordance and a mosaic pattern of alleles derived from either of the putative parental species. The average variation on the Z chromosome was significantly reduced compared with autosomal variation in the putative parental species, the house sparrow and Spanish sparrow. Additionally, divergence between the two species was elevated on the Z chromosome relative to the autosomes. This pattern of variation and divergence is consistent with reduced introgression of Z‐linked genes and/or a faster‐Z effect (increased rate of adaptive divergence on the Z). FST‐outlier tests were consistent with the faster‐Z hypothesis: two of five Z‐linked loci (CHD1Z and PLAA) were identified as candidates for being subject to positive, divergent selection in the putative parental species. Interestingly, the two latter genes showed a mosaic pattern in the (hybrid) Italian sparrow; that is, the Italian sparrow was found to be fixed for Spanish sparrow alleles at CHD1Z and to mainly have house sparrow alleles at PLAA. Preliminary evidence presented in this study thus suggests that sex chromosomes may play a significant role in this case of homoploid hybrid speciation.

Successful by Chance? The Power of Mixed Models and Neutral Simulations for the Detection of Individual Fixed Heterogeneity in Fitness Components

Heterogeneity in fitness components consists of fixed heterogeneity due to latent differences fixed throughout life (e.g., genetic variation) and dynamic heterogeneity generated by stochastic variation. Their relative magnitude is crucial for evolutionary processes, as only the former may allow for adaptation. However, the importance of fixed heterogeneity in small populations has recently been questioned. Using neutral simulations (NS), several studies failed to detect fixed heterogeneity, thus challenging previous results from mixed models (MM). To understand the causes of this discrepancy, we estimate the statistical power and false positive rate of both methods and apply them to empirical data from a wild rodent population. While MM show high false-positive rates if confounding factors are not accounted for, they have high statistical power to detect real fixed heterogeneity. In contrast, NS are also subject to high false-positive rates but always have low power. Indeed, MM analyses of the rodent population data show significant fixed heterogeneity in reproductive success, whereas NS analyses do not. We suggest that fixed heterogeneity may be more common than is suggested by NS and that NS are useful only if more powerful methods are not applicable and if they are complemented by a power analysis.

Bigger is fitter? Quantitative genetic decomposition of selection reveals an adaptive evolutionary decline of body mass in a wild rodent population

In natural populations, quantitative trait dynamics often do not appear to follow evolutionary predictions. Despite abundant examples of natural selection acting on heritable traits, conclusive evidence for contemporary adaptive evolution remains rare for wild vertebrate populations, and phenotypic stasis seems to be the norm. This so-called “stasis paradox” highlights our inability to predict evolutionary change, which is especially concerning within the context of rapid anthropogenic environmental change. While the causes underlying the stasis paradox are hotly debated, comprehensive attempts aiming at a resolution are lacking. Here, we apply a quantitative genetic framework to individual-based long-term data for a wild rodent population and show that despite a positive association between body mass and fitness, there has been a genetic change towards lower body mass. The latter represents an adaptive response to viability selection favouring juveniles growing up to become relatively small adults, i.e., with a low potential adult mass, which presumably complete their development earlier. This selection is particularly strong towards the end of the snow-free season, and it has intensified in recent years, coinciding which a change in snowfall patterns. Importantly, neither the negative evolutionary change, nor the selective pressures that drive it, are apparent on the phenotypic level, where they are masked by phenotypic plasticity and a non causal (i.e., non genetic) positive association between body mass and fitness, respectively. Estimating selection at the genetic level enabled us to uncover adaptive evolution in action and to identify the corresponding phenotypic selective pressure. We thereby demonstrate that natural populations can show a rapid and adaptive evolutionary response to a novel selective pressure, and that explicitly (quantitative) genetic models are able to provide us with an understanding of the causes and consequences of selection that is superior to purely phenotypic estimates of selection and evolutionary change.

A reassessment of explanations for discordant introgressions of mitochondrial and nuclear genomes

Hybridization is increasingly recognized as a significant evolutionary process, in particular because it can lead to introgression of genes from one species to another. A striking pattern of discordance in the amount of introgression between mitochondrial and nuclear markers exists such that substantial mitochondrial introgression is often found in combination with no or little nuclear introgression. Multiple mechanisms have been proposed to explain this discordance, including positive selection for introgressing mitochondrial variants, several types of sex‐biases, drift, negative selection against introgression in the nuclear genome, and spatial expansion. Most of these hypotheses are verbal, and have not been quantitatively evaluated so far. We use individual‐based, multilocus, computer simulations of secondary contact under a wide range of demographic and genetic scenarios to evaluate the ability of the different mechanisms to produce discordant introgression. Sex‐biases and spatial expansions fail to produce substantial mito‐nuclear discordance. Drift and nuclear selection can produce strong discordance, but only under a limited range of conditions. In contrast, selection on the mitochondrial genome produces strong discordance, particularly when dispersal rates are low. However, commonly used statistical tests have little power to detect this selection. Altogether, these results dismiss several popular hypotheses, and provide support for adaptive mitochondrial introgression.

Disentangling evolutionary, plastic and demographic processes underlying trait dynamics: A review of four frameworks

1.Biologists are increasingly interested in decomposing trait dynamics into underlying processes, such as evolution, plasticity and demography. Four important frameworks that allow for such a decomposition are the quantitative genetic animal model (AM), the ‘Geber’ method (GM), the age-structured Price equation (APE), and the integral projection model (IPM). However, as these frameworks have largely been developed independently, they differ in the assumptions they make, the data they require, as well as their outcomes and interpretation. 2.Here we evaluate how each framework decomposes trait dynamics into underlying processes. To do so, we apply them to simulated data for a hypothetical animal population. Individual body size was affected by, among others, genes, maternal effects and food intake. We simulated scenarios with and without selection on body size, and with high and low heritability. 3.The APE and IPM provided similar results, as did the AM and GM, with important differences between the former and the latter. All frameworks detected positive contributions of selection in the high but not in the low selection scenarios. However, only the AM and GM distinguished between the high and low heritability scenarios. Furthermore, the AM and GM revealed a high contribution of plasticity. The APE and IPM attributed most of the change in body size to ontogenetic growth and inheritance, where the latter captures the combined effects of plasticity, maternal effects and heritability. We show how these apparent discrepancies are mostly due to differences in aims and definitions. For example, the APE and IPM capture selection, whereas the AM and GM focus on the response to selection. Furthermore, the frameworks differ in the processes that are ascribed to plasticity and in how they take into account demography. 4.We conclude that no single framework provides the ‘true’ contributions of evolution, plasticity and demography. Instead, different research questions require different frameworks. A thorough understanding of the different definitions of their components is necessary for selecting the most appropriate framework for the question at hand, and for making biologically meaningful inferences. This work thus supports both future analysis as well as the careful interpretation of existing work. This article is protected by copyright. All rights reserved.

Heritability, selection, and the response to selection in the presence of phenotypic measurement error: effects, cures, and the role of repeated measurements

Quantitative genetic analyses require extensive measurements of phenotypic traits, a task that is often not trivial, especially in wild populations. On top of instrumental measurement error, some traits may undergo transient (i.e. non-persistent) fluctuations that are biologically irrelevant for selection processes. These two sources of variability, which we denote here as measurement error in a broad sense, are possible causes for bias in the estimation of quantitative genetic parameters. We illustrate how in a continuous trait transient effects with a classical measurement error structure may bias estimates of heritability, selection gradients, and the predicted response to selection. We propose strategies to obtain unbiased estimates with the help of repeated measurements taken at an appropriate temporal scale. However, the fact that in quantitative genetic analyses repeated measurements are also used to isolate permanent environmental instead of transient effects, requires a re-assessment of the information content of repeated measurements. To do so, we propose to distinguish “short-term” from “long-term” repeats, where the former capture transient variability and the latter the permanent effects. We show how the inclusion of the corresponding variance components in quantitative genetic models yields unbiased estimates of all quantities of interest, and we illustrate the application of the method to data from a Swiss snow vole population.

Fluctuating selection and its (elusive) evolutionary consequences in a wild rodent population

Temporal fluctuations in the strength and direction of selection are often proposed as a mechanism that slows down evolution, both over geological and contemporary timescales. Both the prevalence of fluctuating selection and its relevance for evolutionary dynamics remain poorly understood however, especially on contemporary timescales: unbiased empirical estimates of variation in selection are scarce, and the question of how much of the variation in selection translates into variation in genetic change has largely been ignored. Using long‐term individual‐based data for a wild rodent population, we quantify the magnitude of fluctuating selection on body size. Subsequently, we estimate the evolutionary dynamics of size and test for a link between fluctuating selection and evolution. We show that, over the past 11 years, phenotypic selection on body size has fluctuated significantly. However, the strength and direction of genetic change have remained largely constant over the study period; that is, the rate of genetic change was similar in years where selection favoured heavier vs. lighter individuals. This result suggests that over shorter timescales, fluctuating selection does not necessarily translate into fluctuating evolution. Importantly however, individual‐based simulations show that the correlation between fluctuating selection and fluctuating evolution can be obscured by the effect of drift, and that substantially more data are required for a precise and accurate estimate of this correlation. We identify new challenges in measuring the coupling between selection and evolution, and provide methods and guidelines to overcome them.

Heritability, selection, and the response to selection in the presence of phenotypic measurement error: Effects, cures, and the role of repeated measurements: PHENOTYPIC MEASUREMENT ERROR: EFFECTS AND CURES

Quantitative genetic analyses require extensive measurements of phenotypic traits, a task that is often not trivial, especially in wild populations. On top of instrumental measurement error, some traits may undergo transient (i.e., nonpersistent) fluctuations that are biologically irrelevant for selection processes. These two sources of variability, which we denote here as measurement error in a broad sense, are possible causes for bias in the estimation of quantitative genetic parameters. We illustrate how in a continuous trait transient effects with a classical measurement error structure may bias estimates of heritability, selection gradients, and the predicted response to selection. We propose strategies to obtain unbiased estimates with the help of repeated measurements taken at an appropriate temporal scale. However, the fact that in quantitative genetic analyses repeated measurements are also used to isolate permanent environmental instead of transient effects requires that the information content of repeated measurements is carefully assessed. To this end, we propose to distinguish “short‐term” from “long‐term” repeats, where the former capture transient variability and the latter help isolate permanent effects. We show how the inclusion of the corresponding variance components in quantitative genetic models yields unbiased estimates of all quantities of interest, and we illustrate the application of the method to data from a Swiss snow vole population.

Genetic species identification of a Collared Pied Flycatcher from Norway

One male Ficedula flycatcher, breeding in southeast Norway, was identified in the field as a putative hybrid between the Pied Flycatcher F. hypoleuca and the Collared Flycatcher F. albicollis due to the presence of a partial neck collar and other intermediate plumage traits. The male and his seven nestlings were genotyped using species-diagnostic genetic markers, along with three positive controls of both flycatcher species. The male only possessed Pied Flycatcher alleles, suggesting that it is a pure Pied Flycatcher but with rare plumage characteristics approaching those of a Collared Flycatcher. Partial neck collars are also found in other black-and-white flycatcher species; the Semi-collared Flycatcher F. semitorquata (regularly) and the Atlas Flycatcher F. speculigera (occasionally), and have also been reported to occasionally occur among the Iberian subspecies of the Pied Flycatcher (F. h. iberiae). We suggest that a (partial) neck collar may be the ancestral character state of the common ancestor of these black-and-white flycatcher species, and thus that the trait may also occasionally be expressed in populations that normally lack it. Our study demonstrates that species identification based on morphological cues may sometimes be insufficient, even in species that normally possess species-diagnostic plumage characteristics.ZusammenfassungEin männlicher Ficedula-Fliegenschnäpper, der in Südostnorwegen brütete, wurde im Freiland als vermeintliche Hybride von Trauerschnäpper F. hypoleuca und Halsbandschnäpper F. albicollis identifiziert, da er ein unvollständiges Halsband und andere intermediäre Gefiedermerkmale hatte. Das Männchen und seine sieben Nestlinge wurden unter Verwendung artdiagnostischer genetischer Marker genotypisiert, zusammen mit drei Positivkontrollen beider Fliegenschnäpper-Arten. Das Männchen besaß lediglich Trauerschnäpper-Allele, was darauf hindeutet, dass es sich um einen reinen Trauerschnäpper handelte, jedoch mit seltenen Gefiedermerkmalen, die denen eines Halsbandschnäppers ähneln. Unvollständige Halsbänder findet man auch bei anderen schwarzweißen Fliegenschnäpper-Arten, dem Halbringschnäpper F. semitorquata (regelmäßig) und dem Atlasschnäpper F. speculigera (gelegentlich), und es wurde berichtet, dass sie mitunter bei der iberischen Unterart des Trauerschnäppers (F. h. iberiae) auftreten. Wir schlagen vor, dass ein (unvollständiges) Halsband ein ursprüngliches Kennzeichen des gemeinsamen Vorfahren der schwarzweißen Fliegenschnäpper-Arten sein könnte und daher gelegentlich auch in Populationen exprimiert wird, in denen es normalerweise fehlt. Unsere Studie zeigt, dass eine Artbestimmung auf Grund morphologischer Kennzeichen manchmal unzulänglich sein kann, selbst bei Arten, die normalerweise artdiagnostische Gefiedermerkmale besitzen.