Urban park characteristics, genetic variation, and historical demography of white-footed mouse (Peromyscus leucopus) populations in New York City

Severe fragmentation is a typical fate of native remnant habitats in cities, and urban wildlife with limited dispersal ability are predicted to lose genetic variation in isolated urban patches. However, little information exists on the characteristics of urban green spaces required to conserve genetic variation. In this study, we examine whether isolation in New York City (NYC) parks results in genetic bottlenecks in white-footed mice (Peromyscus leucopus), and test the hypotheses that park size and time since isolation are associated with genetic variability using nonlinear regression and information-theoretic model selection. White-footed mice have previously been documented to exhibit male-biased dispersal, which may create disparities in genetic variation between males and females in urban parks. We use genotypes of 18 neutral microsatellite data and four different statistical tests to assess this prediction. Given that sex-biased dispersal may create disparities between population genetic patterns inferred from bi- vs. uni-parentally inherited markers, we also sequenced a 324 bp segment of the mitochondrial D-loop for independent inferences of historical demography in urban P. leucopus. We report that isolation in urban parks does not necessarily result in genetic bottlenecks; only three out of 14 populations in NYC parks exhibited a signature of a recent bottleneck at 18 neutral microsatellite loci. Mouse populations in larger urban parks, or parks that have been isolated for shorter periods of time, also do not generally contain greater genetic variation than populations in smaller parks. These results suggest that even small networks of green spaces may be sufficient to maintain the evolutionary potential of native species with certain characteristics. We also found that isolation in urban parks results in weak to nonexistent sex-biased dispersal in a species known to exhibit male-biased dispersal in less fragmented environments. In contrast to nuclear loci, mitochondrial D-loop haplotypes exhibited a mutational pattern of demographic expansion after a recent bottleneck or selective sweep. Estimates of the timing of this expansion suggest that it occurred concurrent with urbanization of NYC over the last few dozens to hundreds of years. Given the general non-neutrality of mtDNA in many systems and evidence of selection on related coding sequences in urban P. leucopus, we argue that the P. leucopus mitochondrial genome experienced recent negative selection against haplotypes not favored in isolated urban parks. In general, rapid adaptive evolution driven by urbanization, global climate change, and other human-caused factors is underappreciated by evolutionary biologists, but many more cases will likely be documented in the near future

Asocial Monogamy, Extra-pair Paternity, and Dispersal in the Large Treeshrew (Tupaia tana)

Monogamy occurs in only 5% of mammalian species, but is significantly more common in the Euarchonta: primates, dermopterans, and treeshrews (15% spp.). However, many of these species do not breed monogamously, indicating the need to understand behavioral and genetic monogamy as separate evolutionary phenomena. I examined monogamy in the large treeshrew (Tupaia tana) in Sabah, Malaysia using radiotelemetry data from 46 individuals tracked during and after a fruit masting episode in 1990-1991, during a non-masting period from 2002-2004, and in a selectively logged forest from 2003-2004. I show that large treeshrews exhibit behavioral monogamy in all these ecological situations. However, behavioral monogamy is best characterized as dispersed pair-living, or "asocial monogamy", in this species because male-female pairs travel, forage, and sleep alone on their joint territories. Next, I use microsatellites and mitochondrial DNA d-loop haplotypes to analyze the genetic maternity and paternity of 24 T. tana offspring. I show one of the highest rates of extra-pair paternity (EPP) ever recorded for a behaviorally monogamous mammal. Over 40% of young were sired by males that were not the behavioral partner of their mother, and three litters exhibited evidence of multiple paternity. Comparative analysis of relative testis size in treeshrews and primates indicates that sperm competition is not associated with the high rates of EPP in T. tana, and that the evolution of monogamy is associated with the evolution of smaller testes. Finally, I find genetic evidence of female-biased dispersal and gene flow in large treeshrews. The vast majority of mammals exhibit the behavioral combination of polygyny and male-biased dispersal, but female-biased dispersal may evolve in monogamous species when females compete for ecological resources. In support of the local resource competition hypothesis, I find lower population assignment probabilities and pairwise relatedness for females than males. These results indicate that female T. tana are a mixture of philopatric residents and immigrants from other areas. Coalescent-based Bayesian analyses also show that historical female migration has been three times higher than the overall migration rate between primary and logged forest populations, providing evidence of female-biased gene flow

Harnessing Population Genetics for Pest Management: Theory and Application for Urban Rats

Effective management of rodent pests requires an ecological understanding of how they move through their environment and how those movements influence the invasion, persistence, or reinvasion of problematic colonies. Traditional methodologies used to describe rodent movement patterns, such as mark-recapture, are hindered by their time-consuming nature and limited geographic scope. As such, our understanding of how rodents interact with urban environments remains limited. Population genetic principles and tools have the capacity to greatly increase our understanding of rodent population dynamics, ecological relationships, and movements across space, but this field is often unapproachable to non-scientist pest management professionals (PMPs). In this commentary, we aim to promote collaborative and integrative rodent pest management by introducing relevant population genetic principles, providing examples of their applications in studies of urban brown rats (Rattus norvegicus), and proposing future initiatives that link scientific, private, and government entities. We reinterpret results from a 2018 study of brown rats in Vancouver, British Columbia, Canada to show how genetic relationships among individual brown rats can be used to understand the geographic distribution of genetic clusters (i.e., colonies), natural barriers to migration, and the spatial scale of dispersal. While the 2018 study originally aimed to describe patterns of population genetic structure to understand the influence of urban landscapes on rats, here we describe how these results can be exploited by PMPs to directly inform the creation of management units and decrease the likelihood of rapid post-treatment reinvasion. Further, we discuss the difficulties inherent in population genetic studies and the potential for high-quality model sites to develop generalizable strategies. Overall, we hope to expand the toolbox of PMPs, foster collaboration, and move toward more informed and sustainable management strategies

Conservation genetics of extremely isolated urban populations of the northern dusky salamander (Desmognathus fuscus) in New York City

Urbanization is a major cause of amphibian decline. Stream-dwelling plethodontid salamanders are particularly susceptible to urbanization due to declining water quality and hydrological changes, but few studies have examined these taxa in cities. The northern dusky salamander (Desmognathus fuscus) was once common in the New York City metropolitan area, but has substantially declined throughout the region in recent decades. We used five tetranucleotide microsatellite loci to examine population differentiation, genetic variation, and bottlenecks among five remnant urban populations of dusky salamanders in NYC. These genetic measures provide information on isolation, prevalence of inbreeding, long-term prospects for population persistence, and potential for evolutionary responses to future environmental change. All populations were genetically differentiated from each other, and the most isolated populations in Manhattan have maintained very little genetic variation (i.e. \u3c20% heterozygosity). A majority of the populations also exhibited evidence of genetic bottlenecks. These findings contrast with published estimates of high genetic variation within and lack of structure between populations of other desmognathine salamanders sampled over similar or larger spatial scales. Declines in genetic variation likely resulted from population extirpations and the degradation of stream and terrestrial paths for dispersal in NYC. Loss of genetic variability in populations isolated by human development may be an underappreciated cause and/or consequence of the decline of this species in urbanized areas of the northeast USA

Signatures of Rapid Evolution in Urban and Rural Transcriptomes of White-Footed Mice (Peromyscus leucopus) in the New York Metropolitan Area

Urbanization is a major cause of ecological degradation around the world, and human settlement in large cities is accelerating. New York City (NYC) is one of the oldest and most urbanized cities in North America, but still maintains 20% vegetation cover and substantial populations of some native wildlife. The white-footed mouse, Peromyscus leucopus, is a common resident of NYC’s forest fragments and an emerging model system for examining the evolutionary consequences of urbanization. In this study, we developed transcriptomic resources for urban P. leucopus to examine evolutionary changes in protein-coding regions for an exemplar “urban adapter.” We used Roche 454 GS FLX+ high throughput sequencing to derive transcriptomes from multiple tissues from individuals across both urban and rural populations. From these data, we identified 31,015 SNPs and several candidate genes potentially experiencing positive selection in urban populations of P. leucopus. These candidate genes are involved in xenobiotic metabolism, innate immune response, demethylation activity, and other important biological phenomena in novel urban environments. This study is one of the first to report candidate genes exhibiting signatures of directional selection in divergent urban ecosystems

The evolutionary history of wild and domestic brown rats (Rattus norvegicus)

The brown rat (Rattus norvegicus) occupies nearly every terrestrial habitat with a human presence and is one of our most important model organisms. Despite this prevalence, gaps remain in understanding the evolution of brown rat commensalism, their global dispersal, and mechanisms underlying contemporary adaptations to diverse environments. In this Review, we explore recent advances in the evolutionary history of brown rats and discuss key challenges, including finding and accurately dating historical specimens, disentangling histories of multiple domestication events, and synthesizing functional variation in wild rat populations with the development of laboratory strains. Advances in zooarchaeology and population genomics will usher in a new golden age of research on the evolutionary biology of brown rats, with positive feedbacks on their use as biomedical models

Temporal and Space-Use Changes by Rats in Response to Predation by Feral Cats in an Urban Ecosystem

Feral cats (Felis catus) are predators that cause widespread loss of native wildlife in urban ecosystems. Despite these risks, cats are commonly released as control agents for city rats (Rattus spp.). Cats can influence their prey directly by killing or indirectly through changes to feeding or space-use. However, cats prefer defenseless prey, and there are no data suggesting that cats influence large (>300 g) urban rats. We used a pre-existing radiofrequency identification assay (microchipped rats and field cameras) and ethograms to assess the impact of cats, including temporal and space use patterns, on an active rat colony. From Dec 27, 2017 through May 28, 2018 we captured 306 videos of pre-identified cats and/or rats that shared the same space. There were three instances of predation and 20 stalking events. Logistic regression showed the likelihood of a rat being seen on a particular day is associated with the number of cats seen on the same day (OR = 0.1, p < 0.001) or previous day (OR = 0.15, p < 0.001). Space-use was also impacted. For every additional cat sighting, a rat is 1.19 times more likely to move in the direction of shelter. Our findings of low levels of predation support why ecologists believe the risks to native wildlife outweighs any benefits of releasing cats. Even though rats were less likely to be seen, they simply shifted their movements and remained present in the system. Our findings that cat presence led to fewer rat sightings may explain the common perception of their value as rat-predators despite the associated risks

Dispersal Ability Predicts Spatial Genetic Structure in Native Mammals Persisting across an Urbanization Gradient

As the rate of urbanization continues to increase globally, a growing body of research is emerging that investigates how urbanization shapes the movement—and consequent gene flow—of species in cities. Of particular interest are native species that persist in cities, either as small relict populations or as larger populations of synanthropic species that thrive alongside humans in new urban environments. In this study, we used genomic sequence data (SNPs) and spatially explicit individual‐based analyses to directly compare the genetic structure and patterns of gene flow in two small mammals with different dispersal abilities that occupy the same urbanized landscape to evaluate how mobility impacts genetic connectivity. We collected 215 white‐footed mice (Peromyscus leucopus) and 380 big brown bats (Eptesicus fuscus) across an urban‐to‐rural gradient within the Providence, Rhode Island (U.S.A.) metropolitan area (population =1,600,000 people). We found that mice and bats exhibit clear differences in their spatial genetic structure that are consistent with their dispersal abilities, with urbanization having a stronger effect on Peromyscus mice. There were sharp breaks in the genetic structure of mice within the Providence urban core, as well as reduced rates of migration and an increase in inbreeding with more urbanization. In contrast, bats showed very weak genetic structuring across the entire study area, suggesting a near‐panmictic gene pool likely due to the ability to disperse by flight. Genetic diversity remained stable for both species across the study region. Mice also exhibited a stronger reduction in gene flow between island and mainland populations than bats. This study represents one of the first to directly compare multiple species within the same urban‐to‐rural landscape gradient, an important gap to fill for urban ecology and evolution. Moreover, here we document the impacts of dispersal capacity on connectivity for native species that have persisted as the urban landscape matrix expands

Female-Biased Dispersal and Gene Flow in a Behaviorally Monogamous Mammal, the Large Treeshrew (Tupaia tana)

Background: Female-biased dispersal (FBD) is predicted to occur in monogamous species due to local resource competition among females, but evidence for this association in mammals is scarce. The predicted relationship between FBD and monogamy may also be too simplistic, given that many pair-living mammals exhibit substantial extra-pair paternity. Methodology/Principal Findings: I examined whether dispersal and gene flow are female-biased in the large treeshrew (Tupaia tana) in Borneo, a behaviorally monogamous species with a genetic mating system characterized by high rates (50%) of extra-pair paternity. Genetic analyses provided evidence of FBD in this species. As predicted for FBD, I found lower mean values for the corrected assignment index for adult females than for males using seven microsatellite loci, indicating that female individuals were more likely to be immigrants. Adult female pairs were also less related than adult male pairs. Furthermore, comparison of Bayesian coalescent-based estimates of migration rates using maternally and bi-parentally inherited genetic markers suggested that gene flow is female-biased in T. tana. The effective number of migrants between populations estimated from mitochondrial DNA sequence was three times higher than the number estimated using autosomal microsatellites. Conclusions/Significance: These results provide the first evidence of FBD in a behaviorally monogamous species without mating fidelity. I argue that competition among females for feeding territories creates a sexual asymmetry in the costs an

Global population divergence and admixture of the brown rat (Rattus norvegicus)

Native to China and Mongolia, the brown rat (Rattus norvegicus) now enjoys a worldwide distribution. While black rats and the house mouse tracked the regional development of human agricultural settlements, brown rats did not appear in Europe until the 1500s, suggesting their range expansion was a response to relatively recent increases in global trade. We inferred the global phylogeography of brown rats using 32 k SNPs, and detected 13 evolutionary clusters within five expansion routes. One cluster arose following a southward expansion into Southeast Asia. Three additional clusters arose from two independent eastward expansions: one expansion from Russia to the Aleutian Archipelago, and a second to western North America. Westward expansion resulted in the colonization of Europe from which subsequent rapid colonization of Africa, the Americas and Australasia occurred, and multiple evolutionary clusters were detected. An astonishing degree of fine-grained clustering between and within sampling sites underscored the extent to which urban heterogeneity shaped genetic structure of commensal rodents. Surprisingly, few individuals were recent migrants, suggesting that recruitment into established populations is limited. Understanding the global population structure of R. norvegicus offers novel perspectives on the forces driving the spread of zoonotic disease, and aids in development of rat eradication programmes