Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

A robust sequencing assay of a thousand amplicons for the high-throughput population monitoring of Alpine ibex immunogenetics.

Polymorphism for immune functions can explain significant variation in health and reproductive success within species. Drastic loss in genetic diversity at such loci constitutes an extinction risk and should be monitored in species of conservation concern. However, effective implementations of genome-wide immune polymorphism sets into high-throughput genotyping assays are scarce. Here, we report the design and validation of a microfluidics-based amplicon sequencing assay to comprehensively capture genetic variation in Alpine ibex (Capra ibex). This species represents one of the most successful large mammal restorations recovering from a severely depressed census size and a massive loss in diversity at the major histocompatibility complex (MHC). We analysed 65 whole-genome sequencing sets of the Alpine ibex and related species to select the most representative markers and to prevent primer binding failures. In total, we designed ~1,000 amplicons densely covering the MHC, further immunity-related genes as well as randomly selected genome-wide markers for the assessment of neutral population structure. Our analysis of 158 individuals shows that the genome-wide markers perform equally well at resolving population structure as RAD-sequencing or low-coverage genome sequencing data sets. Immunity-related loci show unexpectedly high degrees of genetic differentiation within the species. Such information can now be used to define highly targeted individual translocations. Our design strategy can be realistically implemented into genetic surveys of a large range of species. In conclusion, leveraging whole-genome sequencing data sets to design targeted amplicon assays allows the simultaneous monitoring of multiple genetic risk factors and can be translated into species conservation recommendations.

Limited mass-independent individual variation in resting metabolic rate in a wild population of snow voles (Chionomys nivalis).

Resting metabolic rate (RMR) is a potentially important axis of physiological adaptation to the thermal environment. However, our understanding of the causes and consequences of individual variation in RMR in the wild is hampered by a lack of data, as well as analytical challenges. RMR measurements in the wild are generally characterized by large measurement errors and a strong dependency on mass. The latter is problematic when assessing the ability of RMR to evolve independently of mass. Mixed models provide a powerful and flexible tool to tackle these challenges, but they have rarely been used to estimate repeatability of mass-independent RMR from field data. We used respirometry to obtain repeated measurements of RMR in a long-term study population of snow voles (Chionomys nivalis) inhabiting an environment subject to large circadian and seasonal fluctuations in temperature. Using both uni- and bivariate mixed models, we quantify individual repeatability in RMR and decompose repeatability into mass-dependent and mass-independent components, while accounting for measurement error. RMR varies among individuals, that is, is repeatable (R = .46) and strongly co-varies with BM. Indeed, much of the repeatability of RMR is attributable to individual variation in BM, and the repeatability of mass-independent RMR is reduced by 41% to R = .27. These empirical results suggest that the evolutionary potential of RMR independent of mass may be severely constrained. This study illustrates how to leverage bivariate mixed models to model field data for metabolic traits, correct for measurement error and decompose the relative importance of mass-dependent and mass-independent physiological variation.

Urban colonization through multiple genetic lenses: The city-fox phenomenon revisited.

Urbanization is driving environmental change on a global scale, creating novel environments for wildlife to colonize. Through a combination of stochastic and selective processes, urbanization is also driving evolutionary change. For instance, difficulty in traversing human-modified landscapes may isolate newly established populations from rural sources, while novel selective pressures, such as altered disease risk, toxicant exposure, and light pollution, may further diverge populations through local adaptation. Assessing the evolutionary consequences of urban colonization and the processes underlying them is a principle aim of urban evolutionary ecology. In the present study, we revisited the genetic effects of urbanization on red foxes (Vulpes vulpes) that colonized Zurich, Switzerland. Through use of genome-wide single nucleotide polymorphisms and microsatellite markers linked to the major histocompatibility complex (MHC), we expanded upon a previous neutral microsatellite study to assess population structure, characterize patterns of genetic diversity, and detect outliers associated with urbanization. Our results indicated the presence of one large evolutionary cluster, with substructure evident between geographic sampling areas. In urban foxes, we observed patterns of neutral and functional diversity consistent with founder events and reported increased differentiation between populations separated by natural and anthropogenic barriers. We additionally reported evidence of selection acting on MHC-linked markers and identified outlier loci with putative gene functions related to energy metabolism, behavior, and immunity. We concluded that demographic processes primarily drove patterns of diversity, with outlier tests providing preliminary evidence of possible urban adaptation. This study contributes to our overall understanding of urban colonization ecology and emphasizes the value of combining datasets when examining evolutionary change in an increasingly urban world.

Resurrecting Darwin's Niata - anatomical, biomechanical, genetic, and morphometric studies of morphological novelty in cattle.

The Niata was a cattle variety from South America that figured prominently in writings on evolution by Charles Darwin. Its shortened head and other aspects of its unusual morphology have been subject of unsettled discussions since Darwin's time. Here, we examine the anatomy, cranial shape, skull biomechanics, and population genetics of the Niata. Our results show that the Niata was a viable variety of cattle and exhibited anatomical differences to known chondrodysplastic forms. In cranial shape and genetic analysis, the Niata occupies an isolated position clearly separated from other cattle. Computational biomechanical model comparison reveals that the shorter face of the Niata resulted in a restricted distribution and lower magnitude of stress during biting. Morphological and genetic data illustrate the acquisition of novelty in the domestication process and confirm the distinct nature of the Niata cattle, validating Darwin's view that it was a true breed.

Pedigree-based inbreeding coefficient explains more variation in fitness than heterozygosity at 160 microsatellites in a wild bird population.

Although the pedigree-based inbreeding coefficient F predicts the expected proportion of an individual's genome that is identical-by-descent (IBD), heterozygosity at genetic markers captures Mendelian sampling variation and thereby provides an estimate of realized IBD. Realized IBD should hence explain more variation in fitness than their pedigree-based expectations, but how many markers are required to achieve this in practice remains poorly understood. We use extensive pedigree and life-history data from an island population of song sparrows (Melospiza melodia) to show that the number of genetic markers and pedigree depth affected the explanatory power of heterozygosity and F, respectively, but that heterozygosity measured at 160 microsatellites did not explain more variation in fitness than F This is in contrast with other studies that found heterozygosity based on far fewer markers to explain more variation in fitness than F Thus, the relative performance of marker- and pedigree-based estimates of IBD depends on the quality of the pedigree, the number, variability and location of the markers employed, and the species-specific recombination landscape, and expectations based on detailed and deep pedigrees remain valuable until we can routinely afford genotyping hundreds of phenotyped wild individuals of genetic non-model species for thousands of genetic markers.

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 microsatellite-based linkage map for song sparrows (Melospiza melodia).

Although linkage maps are important tools in evolutionary biology, their availability for wild populations is limited. The population of song sparrows (Melospiza melodia) on Mandarte Island, Canada, is among the more intensively studied wild animal populations. Its long-term pedigree data, together with extensive genetic sampling, have allowed the study of a range of questions in evolutionary biology and ecology. However, the availability of genetic markers has been limited. We here describe 191 new microsatellite loci, including 160 high-quality polymorphic autosomal, 7 Z-linked and 1 W-linked markers. We used these markers to construct a linkage map for song sparrows with a total sex-averaged map length of 1731 cM and covering 35 linkage groups, and hence, these markers cover most of the 38-40 chromosomes. Female and male map lengths did not differ significantly. We then bioinformatically mapped these loci to the zebra finch (Taeniopygia guttata) genome and found that linkage groups were conserved between song sparrows and zebra finches. Compared to the zebra finch, marker order within small linkage groups was well conserved, whereas the larger linkage groups showed some intrachromosomal rearrangements. Finally, we show that as expected, recombination frequency between linked loci explained the majority of variation in gametic phase disequilibrium. Yet, there was substantial overlap in gametic phase disequilibrium between pairs of linked and unlinked loci. Given that the microsatellites described here lie on 35 of the 38-40 chromosomes, these markers will be useful for studies in this species, as well as for comparative genomics studies with other species.

Identifying Y-chromosomal diversity by long-template PCR.

Comparing Y-chromosomal and mitochondrial haplotype variation is a promising approach to independently investigate paternal and maternal evolutionary histories in wild mammal populations. However, the difficulty of developing male-specific genetic markers, because of its distinctive genetic architecture and the general low level of polymorphisms observed on the Y chromosome, hampers usually an effective application of this approach. Here, we present a further method of the established Y chromosome conserved anchored tagged sequences strategy to develop Y-chromosomal markers by screening introns of male-specific region (MSY) genes for sequence polymorphisms. By applying long-template PCR using target species-specific primers, adequate sequence information of several kb in size can be obtained. We applied this method in the snow vole (Chionomys nivalis) and obtained 12.4 kb of male-specific sequence data for nine males representing four populations in the Swiss Alps. A total of 28 single nucleotide polymorphisms, four indels (> 1 bp) and one polymorphic microsatellite were identified in introns of the SMCY and DBY genes. Based on this information, we developed a Y-chromosomal genotyping assay and identified four different paternal lineages within one local snow vole population. The method we present is straightforward and as such will probably be suitable to detect adequate Y-chromosomal diversity in a wide range of mammalian species.

Monitoring of wild birds for Newcastle disease virus in Switzerland using real time RT-PCR.

Wild birds are considered to be the natural reservoir of the Newcastle disease virus (NDV; avian paramyxovirus-1) causing New-castle disease, and are often suspected to be involved in outbreaks in domesticated birds. To assess the epidemiologic status of wild birds living, or overwintering, in Switzerland, 3,049 cloacal swabs covering the period 2003-2006 were screened for NDV, using real time RT-PCR. All samples were negative. This result seems in contrast with previously performed serologic screenings of wild birds.