Alain C. Frantz

Statistical methods in spatial genetics

The joint analysis of spatial and genetic data is rapidly becoming the norm in population genetics. More and more studies explicitly describe and quantify the spatial organization of genetic variation and try to relate it to underlying ecological processes. As it has become increasingly difficult to keep abreast with the latest methodological developments, we review the statistical toolbox available to analyse population genetic data in a spatially explicit framework. We mostly focus on statistical concepts but also discuss practical aspects of the analytical methods, highlighting not only the potential of various approaches but also methodological pitfalls.

Patterns of crop damage by wild boar (Sus scrofa) in Luxembourg over a 10-year period

In many European countries, the wild boar (Sus scrofa) is often associated with crop damage. In this study, we analyse data relating to 13,276 cases of wild boar damage to agricultural crops over a 10-year period in Luxembourg (an area of 2,586 km2 in Western Europe). Results show that (1) damage is more severe in this area than in others; (2) damage to permanent grassland is far more frequent and more severe than damage to annual crops; (3) trichomatous crops such as barley are avoided; (4) damage is seasonally distributed according to type of crop; (5) damage is distributed spatially in a non-uniform manner; (6) damage intensity is significantly correlated with wild boar hunting bags, both over time and space. We suggest that wild boar management strategy should always take into account the issue of damage to agricultural crops. Our results imply that measures for preventing or reducing damage should be more targeted in time and space and that adjustments to cropping patterns should contribute towards a reduction of wild boar damage.

Genetic structure and assignment tests demonstrate illegal translocation of red deer (Cervus elaphus) into a continuous population

Molecular forensic methods are being increasingly used to help enforce wildlife conservation laws. Using multilocus genotyping, illegal translocation of an animal can be demonstrated by excluding all potential source populations as an individuals population of origin. Here, we illustrate how this approach can be applied to a large continuous population by defining the population genetic structure and excluding suspect animals from each identified cluster. We aimed to test the hypothesis that recreational hunters had illegally introduced a group of red deer into a hunting area in Luxembourg. Reference samples were collected over a large area in order to test the possibility that the suspect individuals might be recent immigrants. Due to isolation‐by‐distance relationships in the data set, inferring the number of genetic clusters using Bayesian methods was not straightforward. Biologically meaningful clusters were only obtained by simultaneously analysing spatial and genetic information using the program baps 4.1. We inferred the presence of three genetic clusters in the study region. Using partial Mantel tests, we detected barriers to gene flow other than distance, probably created by a combination of urban areas, motorways and a river valley used for viticulture. The four focal animals could be excluded with a high certainty from the three genetic subpopulations and it was therefore likely that they had been released illegally.

Independent colonization of multiple urban centres by a formerly forest specialist bird species.

Urban areas are expanding rapidly, but a few native species have successfully colonized them. The processes underlying such colonization events are poorly understood. Using the blackbird Turdus merula, a former forest specialist that is now one of the most common urban birds in its range, we provide the first assessment of two contrasting urban colonization models. First, that urbanization occurred independently. Second, that following initial urbanization, urban-adapted individuals colonized other urban areas in a leapfrog manner. Previous analyses of spatial patterns in the timing of blackbird urbanization, and experimental introductions of urban and rural blackbirds to uncolonized cities, suggest that the leapfrog model is likely to apply. We found that, across the western Palaearctic, urban blackbird populations contain less genetic diversity than rural ones, urban populations are more strongly differentiated from each other than from rural populations and assignment tests support a rural source population for most urban individuals. In combination, these results provide much stronger support for the independent urbanization model than the leapfrog one. If the former model predominates, colonization of multiple urban centres will be particularly difficult when urbanization requires genetic adaptations, having implications for urban species diversity.

Comparative landscape genetic analyses show a Belgian motorway to be a gene flow barrier for red deer (Cervus elaphus), but not wild boars (Sus scrofa)

While motorways are often assumed to influence the movement behaviour of large mammals, there are surprisingly few studies that show an influence of these linear structures on the genetic make‐up of wild ungulate populations. Here, we analyse the spatial genetic structure of red deer (Cervus elaphus) and wild boars (Sus scrofa) along a stretch of motorway in the Walloon part of Belgium. Altogether, 876 red deer were genotyped at 13 microsatellite loci, and 325 wild boars at 14 loci. In the case of the red deer, different genetic clustering tools identified two genetic subpopulations whose borders matched the motorway well. Conversely, no genetic structure was identified in the case of the wild boar. Analysis of isolation‐by‐distance patterns of pairs of individuals on the same side and on different sides of the motorway also suggested that the road was a barrier to red deer, but not to wild boar movement. While telemetry studies seem to confirm that red deer are more affected by motorways than wild boar, the red deer sample size was also much larger than that of the wild boars. We therefore repeated the analysis of genetic structure in the red deer with randomly sub‐sampled data sets of decreasing size. The power to detect the genetic structure using clustering methods decreased with decreasing sample size.

Using isolation-by-distance-based approaches to assess the barrier effect of linear landscape elements on badger (Meles meles) dispersal

As the European badger (Meles meles) can be of conservation or management concern, it is important to have a good understanding of the species’ dispersal ability. In particular, knowledge of landscape elements that affect dispersal can contribute to devising effective management strategies. However, the standard approach of using Bayesian clustering methods to correlate genetic discontinuities with landscape elements cannot easily be applied to this problem, as badger populations are often characterized by a strong confounding isolation‐by‐distance (IBD) pattern. We therefore developed a two‐step method that compares the location of pairs of related badgers relative to a putative barrier and utilizes the expected spatial genetic structure characterized by IBD as a null model to test for the presence of a barrier. If a linear feature disrupts dispersal, the IBD pattern characterising pairs of individuals located on different sides of a putative barrier should differ significantly from the pattern obtained with pairs of individuals located on the same side. We used our new approach to assess the impact of rivers and roads of different sizes on badger dispersal in western England. We show that a large, wide river represented a barrier to badger dispersal and found evidence that a motorway may also restrict badger movement. Conversely, we did not find any evidence for small rivers and roads interfering with badger movement. One of the advantages of our approach is that potentially it can detect features that disrupt gene flow locally, without necessarily creating distinct identifiable genetic units.

Incorporating Genotype Uncertainty into Mark–Recapture-Type Models For Estimating Abundance Using DNA Samples

Sampling DNA noninvasively has advantages for identifying animals for uses such as mark-recapture modeling that require unique identification of animals in samples. Although it is possible to generate large amounts of data from noninvasive sources of DNA, a challenge is overcoming genotyping errors that can lead to incorrect identification of individuals. A major source of error is allelic dropout, which is failure of DNA amplification at one or more loci. This has the effect of heterozygous individuals being scored as homozygotes at those loci as only one allele is detected. If errors go undetected and the genotypes are naively used in mark-recapture models, significant overestimates of population size can occur. To avoid this it is common to reject low-quality samples but this may lead to the elimination of large amounts of data. It is preferable to retain these low-quality samples as they still contain usable information in the form of partial genotypes. Rather than trying to minimize error or discarding error-prone samples we model dropout in our analysis. We describe a method based on data augmentation that allows us to model data from samples that include uncertain genotypes. Application is illustrated using data from the European badger (Meles meles).

Genetic signatures of population change in the British golden eagle (Aquila chrysaetos)

The golden eagle (Aquila chrysaetos) was once widely distributed in the uplands of the British Isles, but is now extinct in Ireland, and largely confined to the highlands and islands of Scotland. As the precise extent and severity of the reduction in population size are unclear, it is important to understand how the population was affected by the decline. We therefore genotyped 13 polymorphic microsatellite loci in 172 individuals from the contemporary British population and compared their genetic diversity to 70 British and 9 Irish museum specimens. Despite the recent population decline, there is only slight evidence for a concomitant loss of genetic variation. Instead, two likelihood-based Bayesian methods provided evidence for a severe ancient genetic bottleneck, possibly caused by the fragmentation of a large mainland European population and/or the founding effects of colonising the British Isles. As the population persisted despite this ancient bottleneck, our conclusion is that there is limited need for intervention to augment the present-day genetic diversity. The main short-term objective of conservation measures should be to increase population sizes by continuous safeguarding of individuals and habitat management. Finally, we also confirmed that, for management purposes, the species should be considered a single population unit and that the extinct Irish population was not differentiated from the British one.

Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest

Despite the classic population genetic view of a population as a network of sub-populations consisting of randomly mating individuals, the mating system and dispersal patterns of social animals affect the distribution of genetic variation on a local scale. The spatially open, forest-dwelling red deer (Cervus elaphus) population at the Petite Pierre National Reserve in north-eastern France is culled annually, with the management aim of maximising the number of adult males in the population, and is a typical example of an exploited red deer population from continental Europe. Through a change in management policy, the number of adult males in the population has increased over time, leading to a reduction in variance of male reproductive success (Bonenfant et al., 2002). In this study, we investigate the fine-scale genetic structure of the population using 14 microsatellite loci and attempt to find evidence for a change in this genetic structure over time. DNA was extracted from bone powder obtained by drilling into antlers and mandibular condyles. DNA was successfully extracted from up to 30-year-old samples, but it was necessary to genotype samples in duplicate to obtain reliable genetic profiles. Our results point towards a pattern of fine-scale spatial structure amongst female red deer in the study area, but not amongst males, as would be expected for a typical mammalian system with male-biased dispersal and female philopatry. In addition, our results hint at a decrease in spatial genetic structure amongst females over time, which might be related to a change in management policy, but small sample size limited the robustness of this conclusion.

Revisiting the phylogeography and demography of European badgers (Meles meles) based on broad sampling, multiple markers and simulations

Although the phylogeography of European mammals has been extensively investigated since the 1990s, many studies were limited in terms of sampling distribution, the number of molecular markers used and the analytical techniques employed, frequently leading to incomplete postglacial recolonisation scenarios. The broad-scale genetic structure of the European badger (Meles meles) is of interest as it may result from historic restriction to glacial refugia and/or recent anthropogenic impact. However, previous studies were based mostly on samples from western Europe, making it difficult to draw robust conclusions about the location of refugia, patterns of postglacial expansion and recent demography. In the present study, continent-wide sampling and analyses with multiple markers provided evidence for two glacial refugia (Iberia and southeast Europe) that contributed to the genetic variation observed in badgers in Europe today. Approximate Bayesian computation provided support for a colonisation of Scandinavia from both Iberian and southeastern refugia. In the whole of Europe, we observed a decline in genetic diversity with increasing latitude, suggesting that the reduced diversity in the peripheral populations resulted from a postglacial expansion processes. Although MSVAR v.1.3 also provided evidence for recent genetic bottlenecks in some of these peripheral populations, the simulations performed to estimate the method’s power to correctly infer the past demography of our empirical populations suggested that the timing and severity of bottlenecks could not be established with certainty. We urge caution against trying to relate demographic declines inferred using MSVAR with particular historic or climatological events.