Urban population genetics of slum‐dwelling rats (Rattus norvegicus) in Salvador,Brazil

Throughout the developing world, urban centres with sprawling slum settlements are rapidly expanding and invading previously forested ecosystems. Slum communities are characterized by untended refuse, open sewers and overgrown vegetation, which promote rodent infestation. Norway rats (Rattus norvegicus) are reservoirs for epidemic transmission of many zoonotic pathogens of public health importance. Understanding the population ecology of R. norvegicus is essential to formulate effective rodent control strategies, as this knowledge aids estimation of the temporal stability and spatial connectivity of populations. We screened for genetic variation, characterized the population genetic structure and evaluated the extent and patterns of gene flow in the urban landscape using 17 microsatellite loci in 146 rats from nine sites in the city of Salvador, Brazil. These sites were divided between three neighbourhoods within the city spaced an average of 2.7 km apart. Surprisingly, we detected very little relatedness among animals trapped at the same site and found high levels of genetic diversity, as well as structuring across small geographical distances. Most F_ST comparisons among sites were statistically significant, including sites <400 m apart. Bayesian analyses grouped the samples in three genetic clusters, each associated with distinct sampling sites from different neighbourhoods or valleys within neighbourhoods. These data indicate the existence of complex genetic structure in R. norvegicus in Salvador, linked to the heterogeneous urban landscape. Future rodent control measures need to take into account the spatial and temporal linkage of rat populations in Salvador, as revealed by genetic data, to develop informed eradication strategies.     

Unexpected persistence on habitat islands: genetic signatures reveal dispersal of a eucalypt-dependent marsupial through a hostile pine matrix

Several factors contribute to the extinction of populations in fragmented habitat but key ones include habitat loss and disruptions to connectivity. Aspects of the ecology of greater gliders (Petauroides volans), along with observations of their response to native forest clearance at a site in southeastern Australia, lead to the prediction in the 1960s that the species would not persist in the replacement exotic pine plantation. However, 35 years later, the species was observed in many remnant native vegetation patches retained within the plantation boundary, albeit at a lower occupancy rate than at matched continuous forest control sites. To determine the role of patch connectivity in persistence of P. volans in remnants, we employed 12 microsatellite markers to genotype individuals from 11 remnants, three contemporary nearby continuous native eucalypt forest sites and a sample collected during native vegetation clearance at the site in the 1960s. Patch samples retained substantially more genetic diversity than expected under an isolation model, suggesting that patches have experienced some immigration. Five putative patch immigrants--two from sampled sites 1- and 7-km distant, and three from unresolved or unsampled localities--were identified via genetic parentage and population assignment analyses. Patch populations displayed varying levels of admixture in Bayesian genetic structure analyses, with the oldest and most geographically isolated ones showing the least admixture, suggesting they have experienced relatively little immigration. Evidence of at least some immigration into patches may explain why P. volans has persisted contrary to expectation in heavily fragmented habitat.     

Isolation and characterization of microsatellite loci in the dark bush cricket,Pholidoptera griseoaptera (Tettigoniidae)

Twelve novel polymorphic microsatellite loci are presented for the dark bush cricket, Pholidoptera griseoaptera. All loci are polymorphic, with up to 37 alleles per locus. These microsatellites will be useful tools for studying the influence of landscape structure and land use intensity in agricultural landscapes on genetic diversity within and among populations of P. griseoaptera.     

Rapid,pervasive genetic differentiation of urban white‐footed mouse (Peromyscus leucopus) populations in New York City

We investigated genetic diversity and structure of urban white‐footed mouse, Peromyscus leucopus, populations in New York City (NYC) using variation at 18 microsatellite loci. White‐footed mice are ‘urban adapters’ that occur at higher population densities as habitat fragments are reduced in area but have a limited ability to disperse through urbanized areas. We hypothesized that this combination of traits has produced substantial genetic structure but minimal loss of genetic variation over the last century in NYC. Allelic diversity and heterozygosity in 14 NYC populations were high, and nearly all of our NYC study sites contained genetically distinct populations of white‐footed mice as measured by pairwise F_ST, assignment tests, and Bayesian clustering analyses performed by Structure and baps . Analysis of molecular variance revealed that genetic differences between populations separated by a few kilometres are more significant than differences between prehistorically isolated landmasses (i.e. Bronx, Queens, and Manhattan). Allele size permutation tests and lack of isolation by distance indicated that mutation and migration are less important than drift as explanations for structure in urban, fragmented P. leucopus populations. Peromyscus often exhibit little genetic structure over even regional scales, prompting us to conclude that urbanization is a particularly potent driver of genetic differentiation compared to natural fragmentation.     

Different landscape effects on the genetic structure of two broadly distributed woody legumes,Acacia salicina and A. stenophylla (Fabaceae)

Restoring degraded landscapes has primarily focused on re‐establishing native plant communities. However, little is known with respect to the diversity and distribution of most key revegetation species or the environmental and anthropogenic factors that may affect their demography and genetic structure. In this study, we investigated the genetic structure of two widespread Australian legume species (Acacia salicina and Acacia stenophylla) in the Murray–Darling Basin (MDB), a large agriculturally utilized region in Australia, and assessed the impact of landscape structure on genetic differentiation. We used AFLP genetic data and sampled a total of 28 A. salicina and 30 A. stenophylla sampling locations across southeastern Australia. We specifically evaluated the importance of four landscape features: forest cover, land cover, water stream cover, and elevation. We found that both species had high genetic diversity (mean percentage of polymorphic loci, 55.1% for A. salicina versus. 64.3% for A. stenophylla) and differentiation among local sampling locations (A. salicina: Φ_PT = 0.301, 30%; A. stenophylla: Φ_PT = 0.235, 23%). Population structure analysis showed that both species had high levels of structure (6 clusters each) and admixture in some sampling locations, particularly A. stenophylla. Although both species have a similar geographic range, the drivers of genetic connectivity for each species were very different. Genetic variation in A. salicina seems to be mainly driven by geographic distance, while for A. stenophylla, land cover appears to be the most important factor. This suggests that for the latter species, gene flow among populations is affected by habitat fragmentation. We conclude that these largely co‐occurring species require different management actions to maintain population connectivity. We recommend active management of A. stenophylla in the MDB to improve gene flow in the adversity of increasing disturbances (e.g., droughts) driven by climate change and anthropogenic factors.     

Population genetic structure and dispersal across a fragmented landscape in cerulean warblers (<Emphasis Type="Italic">Dendroica cerulea</Emphasis>)

Cerulean warblers (Dendroica cerulea) have experienced significant declines across their breeding range and presently exist in disjunct populations, largely because of extensive loss and fragmentation of their breeding and wintering habitat. Despite this overall decline, a recent north-eastern expansion of the breeding range has been proposed, and some researchers have suggested that the eastern Ontario population may be acting as a source population maintaining sink populations elsewhere. However, little is known about either the geographic distribution of genetic variation or dispersal in these birds. We assayed variation in five microsatellite loci and a 366 base-pair fragment of the mitochondrial control region among 154 cerulean warblers from five populations throughout the breeding range. No evidence of population genetic structure was found. Assignment tests suggested that six individuals were either inter-population migrants or descendants of recent migrants. The lack of population genetic structure is probably due to a combination of historical association and contemporary dispersal. Population decline does not appear to have reduced genetic variation yet. Overall results suggest that cerulean warblers from Ontario, Illinois, Arkansas and Tennessee should be considered a single genetic management unit for conservation.     

Population genetic effects of urban habitat fragmentation in the perennial herb Viola pubescens (Violaceae) using ISSR markers

BACKGROUND AND AIMS: Fragmentation of natural habitats can negatively impact plant populations by leading to reduced genetic variation and increased genetic distance as populations become geographically and genetically isolated from one another. To test whether such detrimental effects occur within an urban landscape, the genetic structure of six populations of the perennial herb Viola pubescens was characterized in the metropolitan area of Greater Cincinnati in southwestern Ohio, USA. METHODS: Using three inter-simple sequence repeat (ISSR) markers, 51 loci amplified across all urban populations. For reference, four previously examined agricultural populations in central/northern Ohio and a geographically distant population in Michigan were also included in the analysis. KEY RESULTS: Urban populations retained high levels of genetic variation (percentage of polymorphic loci, P(p) = 80.7 %) with similar genetic distances among populations and an absence of unique alleles. Geographic and genetic distances were correlated with one another, and all populations grouped according to region. Individuals from urban populations clustered together and away from individuals from agricultural populations and from the Michigan population in a principle coordinates analysis. Hierarchical analysis of molecular variance (AMOVA) revealed that most of the genetic variability was partitioned within populations (69.1 %) and among groups (22.2 %) of southwestern Ohio, central/northern Ohio and Michigan groups. Mean F(st) was 0.308, indicating substantial population differentiation. CONCLUSIONS: It is concluded that urban fragmentation does not appear to impede gene flow in V. pubescens in southwestern Ohio. These results are consistent with life history traits of this species and the possibility of high insect abundance in urban habitats due to diverse floral resources and nesting sites. Combined with the cleistogamous breeding system of this species, pollinator availability in the urban matrix may buffer populations against detrimental effects of habitat fragmentation, at least in larger forest fragments. Consequently, it may be inappropriate to generalize about genetic effects of fragmentation across landscapes or even across plant species with different pollination systems.     

Genetic diversity of Andean Polylepis (Rosaceae) woodlands and inferences regarding their fragmentation history

There is a long‐standing debate on whether the occurrence of the iconic high‐Andes Polylepis woodlands as small and isolated fragments is of natural or anthropogenic origin. We make inferences regarding the fragmentation history based on both a new population genetic study on P. besseri and a synthesis of available studies on the population genetics of Polylepis woodlands. We infer the timing of the main woodland fragmentation event by analysing: (1) the remaining levels of population genetic diversity and the relation to population size; (2) among‐population genetic differentiation; and (3) the difference in genetic diversity between the offspring and adult generation. We retrieved seven publications on the population genetics of five Polylepis spp. We did not find a relationship between population size and genetic diversity, and genetic differentiation was low compared with that reported for similar plant species. These findings do not support a history of long‐term fragmentation. The offspring showed a loss of genetic diversity and increasing differentiation compared with adults, suggesting that the main habitat fragmentation event is of relatively recent origin. For P. besseri, no significant differences were found between the adult and offspring genetic variation. We discuss the conservation and restoration consequences for this important high‐Andean genus. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 172 , 544–554.     

Shelter availability and human attitudes as drivers of rock hyrax (Procavia capensis) expansion along a rural–urban gradient

While anthropogenic land‐use changes threaten wildlife globally, some species take advantage of such changes and disperse into urban areas. The wildlife in urban areas often promotes conflicts with humans, notably when the animals are associated with the spread of zoonotic diseases. In Israel, current urban invasion of rock hyraxes (Procavia capensis) draws public attention, since the species is a reservoir host of cutaneous leishmaniasis, a serious skin disease. The rock hyrax, however, has seldom been studied in densely populated areas, and the drivers for its urban expansion, as well as its abilities to live and spread in core urban areas, are relatively unknown. Here, we explore the rock hyrax expansion to urban areas process by examining the availability, characteristics and use of shelter along an urban gradient. Our findings suggest that a series of factors determines shelter availability and quality for the rock hyrax, which facilitates its dispersion across the urban gradient. We found that rock hyraxes from the Judean Desert expand to the peri‐urban region of Jerusalem by colonizing new rocky shelters formed as by‐products of urban development. With their populations reaching extreme densities in this area and saturating the available shelters, there is some spill over to the adjacent core urban areas where they colonize littered sites, which are made available due to the local socio‐economic conditions and cultural norms of waste disposal and illegal placement of temporary structures. Our work emphasizes the significance of the urban gradient approach for studying the mechanisms promoting wildlife expansion to cities. Our findings suggest that changes in shelter availability and quality due to urban development, and cultural norms promote shifts of the hyrax population by pushing from the already established areas and pulling into new environment across the urban gradient.     

景观遗传学原理及其在生境片断化遗传效应研究中的应用

景观遗传学是近年来在景观生态学和种群遗传学之间形成的一个交叉领域,强调景观的组成、空间构型和环境梯度对基因流、种群遗传空间结构和局域种群适应的影响。景观遗传学尚未成为一门独立的学科,其理论基础主要来自分子遗传学、种群生物学和景观生态学。现代分子遗传标记技术、遥感和GIS支持下的景观分析和空间统计方法的综合运用是景观遗传学主要研究途径。系统介绍了景观遗传学的基础概念,关键科学问题,基本理论框架,及其与相邻研究领域的关系,综述了景观遗传学最为关注的现实课题——景观碎裂化的种群遗传效应的研究进展,主要涉及生境片断化的遗传效应、不同属性的物种响应、以及生境片断化过程的选择作用等方面。通过采取一种跨尺度的视角,景观遗传学研究显著深化了关于景观碎裂化对生物多样性影响的理解。     

Anthropogenic fragmentation may not alter pre‐existing patterns of genetic diversity and differentiation in perennial shrubs

Many plant species have pollination and seed dispersal systems and evolutionary histories that have produced strong genetic structuring. These genetic patterns may be consistent with expectations following recent anthropogenic fragmentation, making it difficult to detect fragmentation effects if no prefragmentation genetic data are available. We used microsatellite markers to investigate whether severe habitat fragmentation may have affected the structure and diversity of populations of the endangered Australian bird‐pollinated shrub Grevillea caleyi R.Br., by comparing current patterns of genetic structure and diversity with those of the closely related G. longifolia R.Br. that has a similar life history but has not experienced anthropogenic fragmentation. Grevillea caleyi and G. longifolia showed similar and substantial population subdivision at all spatial levels (global F′_ST = 0.615 and 0.454; S_p = 0.039 and 0.066), marked isolation by distance and large heterozygous deficiencies. These characteristics suggest long‐term effects of inbreeding in self‐compatible species that have poor seed dispersal, limited connectivity via pollen flow and undergo population bottlenecks because of periodic fires. Highly structured allele size distributions, most notably in G. caleyi, imply historical processes of drift and mutation were important in isolated subpopulations. Genetic diversity did not vary with population size but was lower in more isolated populations for both species. Through this comparison, we reject the hypothesis that anthropogenic fragmentation has impacted substantially on the genetic composition or structure of G. caleyi populations. Our results suggest that highly self‐compatible species with limited dispersal may be relatively resilient to the genetic changes predicted to follow habitat fragmentation.     

Evaluating the influence of life‐history characteristics on genetic structure: a comparison of small mammals inhabiting complex agricultural landscapes

Conversion of formerly continuous native habitats into highly fragmented landscapes can lead to numerous negative demographic and genetic impacts on native taxa that ultimately reduce population viability. In response to concerns over biodiversity loss, numerous investigators have proposed that traits such as body size and ecological specialization influence the sensitivity of species to habitat fragmentation. In this study, we examined how differences in body size and ecological specialization of two rodents (eastern chipmunk; Tamias striatus and white‐footed mouse; Peromyscus leucopus) impact their genetic connectivity within the highly fragmented landscape of the Upper Wabash River Basin (UWB), Indiana, and evaluated whether landscape configuration and complexity influenced patterns of genetic structure similarly between these two species. The more specialized chipmunk exhibited dramatically more genetic structure across the UWB than white‐footed mice, with genetic differentiation being correlated with geographic distance, configuration of intervening habitats, and complexity of forested habitats within sampling sites. In contrast, the generalist white‐footed mouse resembled a panmictic population across the UWB, and no landscape factors were found to influence gene flow. Despite the extensive previous work in abundance and occupancy within the UWB, no landscape factor that influenced occupancy or abundance was correlated with genetic differentiation in either species. The difference in predictors of occupancy, abundance, and gene flow suggests that species‐specific responses to fragmentation are scale dependent.     

Isolation and characterization of microsatellite loci in Geum urbanum (Rosaceae) and their transferability within the genus Geum

Thirteen novel polymorphic microsatellite loci are presented for Geum urbanum (Rosaceae). The microsatellites will be useful tools to analyse the influence of landscape structure and land‐use intensity in agricultural landscapes on genetic diversity within and among populations of Geum urbanum. Transferability was tested in 19 other Geum species and two Waldsteinia species. In most species polymerase chain reaction (PCR) products of the expected range were obtained, therefore the markers reported here appear to be applicable across the whole genus.     

Impact of habitat fragmentation on the genetics of populations in dendritic landscapes

1. The effect of habitat fragmentation on freshwater species has been addressed using brown trout Salmo trutta L. as a model species with a dendritic population structure. 2. Microsatellite loci were employed as molecular markers. Levels of gene flow and population subdivision were determined in more than 1200 brown trout individuals inhabiting four south European rivers with contrasting patterns of fragmentation, defined by the presence of barriers. 3. The genetic units in the four rivers were restricted by artificial barriers, and gene flow among samples within each river was associated with the level of fragmentation of the river. 4. Loss of genetic diversity and dislocation of the dendritic model have been detected in fragmented rivers. These results emphasise the importance of mitigating the impact of dams by constructing passages to restore gene flow along the river, for fish and other migratory species, as well as the need for caution in relation to stocking in isolated areas to avoid problems of inbreeding.     

Variations in the diet of introduced Norway rats (Rattus norvegicus) inferred using stable isotope analysis

The presence of introduced Norway rats Rattus norvegicus has raised concerns for the fate of the large least auklet Aethia pusilla colony situated at Sirius Point, Kiska Island, Alaska. Previous studies have documented extreme interannual variation in least auklet reproductive success and potential drastic population declines, both of which have been attributed to the varying abundance of, and predation by, Norway rats. A diet study would resolve the uncertainty that remains about the role of rats in the auklet's reproductive failure and the colony's decline. Our main objectives here were to quantify the variation in diet of introduced Norway rats and assess predation on least auklets. Using stable isotope analysis we document wide variability in rat diet dependent on location and provide direct evidence that Norway rats are preferentially preying on least auklets at Sirius Point. In conclusion, we hypothesize that the observed wide variability in rat diet will contribute to the persistence of rats on Kiska long after auklets have been extirpated. The persistence of rats enabled by their foraging plasticity will increase their effects by creating ecological traps within which prospecting individuals will fall and be depredated. This has large conservation consequences as it suggests that when seabirds are extirpated recolonization by prospecting birds is virtually impossible and island ecosystems will continue to be negatively affected and altered as long as introduced predators, such as rats, remain within them.     

Isolation and characterization of highly polymorphic microsatellite markers in Hypochaeris radicata (Asteraceae)

We developed five highly polymorphic dinucleotide microsatellite loci for the grassland species Hypochaeris radicata (Asteraceae). Polymorphism of these markers was examined in six populations in the Netherlands. All loci were polymorphic in all populations. The number of alleles per locus varied between 18 and 43. Expected heterozygosity was between 0.86 and 0.91. Cross‐species amplification was tested in six Hypochaeris species and was successful for three different loci in four species. These microsatellites are a useful tool in population genetic, dispersal and metapopulation studies or in testing levels of inbreeding.     

The influence of landscape structure on occurrence, abundance and genetic diversity of the common frog, Rana temporaria

Human‐caused habitat destruction and modification constitute one of the largest threats to population persistence and biodiversity, and are also suspected to be the major cause behind the global decline of amphibian populations. We assessed the potential role of agriculture‐related habitat fragmentation on population size and genetic variability in the common frog (Rana temporaria) by recording the occurrence, population density and genetic diversity in three geographically disparate regions in Sweden – each containing landscapes of high and low agricultural activity – and related these to landscape variables extracted from digital maps. We found a highly significant region‐by‐landscape interaction in occurrence, population density and genetic diversity revealing a reversed response to agriculture from south to north: while the effects of agriculture on R. temporaria populations were negative in the south, there were no effects in the central region, whereas positive effects were observed in the north. Spatial autocorrelation analyses of genetic data revealed that populations in high agricultural activity areas were more isolated than populations in low activity areas both in the southern and central regions of Sweden. Landscape diversity showed a strong positive correlation with both density and occurrence of frogs in Sweden as a whole, as well as in the southern region. Also, negative effects of roads and positive effects of ditches on genetic diversity were found in the south. Overall, these results suggest clear but regionally opposite effects of habitat structure on the population size and genetic diversity of amphibian populations. This means that the management strategy aiming to maximize the size and genetic diversity of local common frog populations, and perhaps also those of other amphibian populations, should account for regional differences in existing land‐use patterns.     

Habitat distribution influences dispersal and fine-scale genetic population structure of eastern foxsnakes (Mintonius gloydi) across a fragmented landscape

Dispersal is a fundamental attribute of species in nature and shapes population dynamics, evolutionary trajectories and genetic variation across spatial and temporal scales. It is increasingly clear that landscape features have large impacts on dispersal patterns. Thus, understanding how individuals and species move through landscapes is essential for predicting impacts of landscape alterations. Information on dispersal patterns, however, is lacking for many taxa, particularly reptiles. Eastern foxsnakes (Mintoinus gloydi) are marsh and prairie specialists that avoid agricultural fields, but they have persisted across a fragmented region in southwestern Ontario and northern Ohio. Here, we combined habitat suitability modelling with population genetic analyses to infer how foxsnakes disperse through a habitat mosaic of natural and altered landscape features. Boundary regions between the eight genetic clusters, identified through assignment tests, were comprised of low suitability habitat (e.g. agricultural fields). Island populations were grouped into a single genetic cluster, and comparatively low F(ST) values between island and mainland populations suggest open water presents less of a barrier than nonsuitable terrestrial habitat. Isolation by resistance and least-cost path analysis produced similar results with matrices of pairwise individual genetic distance significantly more correlated to matrices of resistance values derived from habitat suitability than models with an undifferentiated landscape. Spatial autocorrelation results matched better with assignment results when incorporating resistance values rather than straight-line distances. All analyses used in our study produced similar results suggesting that habitat degradation limits dispersal for foxsnakes, which has had a strong effect on the genetic population structure across this region.