Jason Munshi-South

Urban landscape genetics: canopy cover predicts gene flow between white‐footed mouse (Peromyscus leucopus) populations in New York City

In this study, I examine the influence of urban canopy cover on gene flow between 15 white‐footed mouse (Peromyscus leucopus) populations in New York City parklands. Parks in the urban core are often highly fragmented, leading to rapid genetic differentiation of relatively nonvagile species. However, a diverse array of ‘green’ spaces may provide dispersal corridors through ‘grey’ urban infrastructure. I identify urban landscape features that promote genetic connectivity in an urban environment and compare the success of two different landscape connectivity approaches at explaining gene flow. Gene flow was associated with ‘effective distances’ between populations that were calculated based on per cent tree canopy cover using two different approaches: (i) isolation by effective distance (IED) that calculates the single best pathway to minimize passage through high‐resistance (i.e. low canopy cover) areas, and (ii) isolation by resistance (IBR), an implementation of circuit theory that identifies all low‐resistance paths through the landscape. IBR, but not IED, models were significantly associated with three measures of gene flow (Nm from FST, BayesAss+ and Migrate‐n) after factoring out the influence of isolation by distance using partial Mantel tests. Predicted corridors for gene flow between city parks were largely narrow, linear parklands or vegetated spaces that are not managed for wildlife, such as cemeteries and roadway medians. These results have implications for understanding the impacts of urbanization trends on native wildlife, as well as for urban reforestation efforts that aim to improve urban ecosystem processes.

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 FST, 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.

Bats and birds: Exceptional longevity despite high metabolic rates

Bats and birds live substantially longer on average than non-flying mammals of similar body size. The combination of small body size, high metabolic rates, and long lifespan in bats and birds would not seem to support oxidative theories of ageing that view senescence as the gradual accumulation of damage from metabolic byproducts. However, large-scale comparative analyses and laboratory studies on a few emerging model species have identified multiple mechanisms for resisting oxidative damage to mitochondrial DNA and cellular structures in both bats and birds. Here we review these recent findings, and suggest areas in which additional progress on ageing mechanisms can be made using bats and birds as novel systems. New techniques for determining the age of free-living, wild individuals, and robustly supported molecular phylogenies, are under development and will improve the efforts of comparative biologists to identify ecological and evolutionary factors promoting long lifespan. In the laboratory, greater development of emerging laboratory models and comparative functional genomic approaches will be needed to identify the molecular pathways of longevity extension in birds and bats.

Evolution of life in urban environments

Welcome to the city Human populations are shifting en masse to cities, which is leading to rapid increases in the number and extent of urban areas. Such changes are well known to cause declines in many species, but they can also act as alternative selection pressures to which some species are able to adapt. Johnson and Munshi-South review the suite of pressures that urban environments exert, the ways in which species may (or may not) adapt, and the larger impact of these evolutionary events on natural processes and human populations. Understanding such urban evolution patterns will improve our ability to foster species persistence in the face of urbanization and to mitigate some of the challenges, such as disease, that adaptation can bring. Science, this issue p. eaam8327 BACKGROUND The extent of urban areas is increasing around the world, and most humans now live in cities. Urbanization results in dramatic environmental change, including increased temperatures, more impervious surface cover, altered hydrology, and elevated pollution. Urban areas also host more non-native species and reduced abundance and diversity of many native species. These environmental changes brought by global urbanization are creating novel ecosystems with unknown consequences for the evolution of life. Here, we consider how early human settlements led to the evolution of human commensals, including some of the most notorious pests and disease vectors. We also comprehensively review how contemporary urbanization affects the evolution of species that coinhabit cities. ADVANCES A recent surge of research shows that urbanization affects both nonadaptive and adaptive evolution. Some of the clearest results of urban evolution show that cities elevate the strength of random genetic drift (stochastic changes in allele frequencies) and restrict gene flow (the movement of alleles between populations due to dispersal and mating). Populations of native species in cities often represent either relicts that predate urbanization or populations that established after a city formed. Both scenarios frequently result in a loss of genetic diversity within populations and increased differentiation between populations. Fragmentation and urban infrastructure also create barriers to dispersal, and consequently, gene flow is often reduced among city populations, which further contributes to genetic differentiation between populations. The influence of urbanization on mutation and adaptive evolution are less clear. A small number of studies suggest that industrial pollution can elevate mutation rates, but the pervasiveness of this effect is unknown. A better studied phenomenon are the effects of urbanization on evolution by natural selection. A growing number of studies show that plant and animal populations experience divergent selection between urban and nonurban environments. This divergent selection has led to adaptive evolution in life history, morphology, physiology, behavior, and reproductive traits. These adaptations typically evolve in response to pesticide use, pollution, local climate, or the physical structure of cities. Despite these important results, the genetic basis of adaptive evolution is known from only a few cases. Most studies also examine only a few populations in one city, and experimental validation is rare. OUTLOOK The study of evolution in urban areas provides insights into both fundamental and applied problems in biology. The thousands of cities throughout the world share some features while differing in other aspects related to their age, historical context, governmental policies, and local climate. Thus, the phenomenon of global urbanization represents an unintended but highly replicated global study of experimental evolution. We can harness this global urban experiment to understand the repeatability and pace of evolution in response to human activity. Among the most important unresolved questions is, how often do native and exotic species adapt to the particular environmental challenges found in cities? Such adaptations could be the difference as to whether a species persists or vanishes from urban areas. In this way, the study of urban evolution can help us understand how evolution in populations may contribute to conservation of rare species, and how populations can be managed to facilitate the establishment of resilient and sustainable urban ecosystems. In a similar way, understanding evolution in urban areas can lead to improved human health. For example, human pests frequently adapt to pesticides and evade control efforts because of our limited understanding of the size of populations and movement of individuals. Applied evolutionary studies could lead to more effective mitigation of pests and disease agents. The study of urban evolution has rapidly become an important frontier in biology, with implications for healthy and sustainable human populations in urban ecosystems. A gradient in urbanization showing the skyline of Canada’s sixth largest city (Mississauga, Canada) on the horizon, and the Credit Valley and the University of Toronto Mississauga campus in the foreground. PHOTO CREDIT: ARJUN YADAV Our planet is an increasingly urbanized landscape, with over half of the human population residing in cities. Despite advances in urban ecology, we do not adequately understand how urbanization affects the evolution of organisms, nor how this evolution may affect ecosystems and human health. Here, we review evidence for the effects of urbanization on the evolution of microbes, plants, and animals that inhabit cities. Urbanization affects adaptive and nonadaptive evolutionary processes that shape the genetic diversity within and between populations. Rapid adaptation has facilitated the success of some native species in urban areas, but it has also allowed human pests and disease to spread more rapidly. The nascent field of urban evolution brings together efforts to understand evolution in response to environmental change while developing new hypotheses concerning adaptation to urban infrastructure and human socioeconomic activity. The next generation of research on urban evolution will provide critical insight into the importance of evolution for sustainable interactions between humans and our city environments.

Population genomics of the Anthropocene: urbanization is negatively associated with genome-wide variation in white-footed mouse populations.

Urbanization results in pervasive habitat fragmentation and reduces standing genetic variation through bottlenecks and drift. Loss of genomewide variation may ultimately reduce the evolutionary potential of animal populations experiencing rapidly changing conditions. In this study, we examined genomewide variation among 23 white‐footed mouse (Peromyscus leucopus) populations sampled along an urbanization gradient in the New York City metropolitan area. Genomewide variation was estimated as a proxy for evolutionary potential using more than 10 000 single nucleotide polymorphism (SNP) markers generated by ddRAD‐Seq. We found that genomewide variation is inversely related to urbanization as measured by percent impervious surface cover, and to a lesser extent, human population density. We also report that urbanization results in enhanced genomewide differentiation between populations in cities. There was no pattern of isolation by distance among these populations, but an isolation by resistance model based on impervious surface significantly explained patterns of genetic differentiation. Isolation by environment modeling also indicated that urban populations deviate much more strongly from global allele frequencies than suburban or rural populations. This study is the first to examine loss of genomewide SNP variation along an urban‐to‐rural gradient and quantify urbanization as a driver of population genomic patterns.

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.

Urban ecology: advancing science and society

Urban ecology has quickly become established as a central part of ecological thinking. As cities continue to grow in size and number, two questions serve to unify this broad and multidisciplinary research landscape: (1) how can urban ecology contribute to the science of ecology, and (2) how can urban ecology be applied to make cities more livable and sustainable? In spite of the advances made thus far, there are many unexplored ways of integrating the science and application of urban ecology. Although scientists assess and make predictions regarding the connections between environmental and socioeconomic processes, practitioners involved in real-world application deal with urban planning and with designing ecosystem services to improve living conditions for all urban inhabitants and to make cities more sustainable. Research in urban ecosystems can be developed from many different perspectives, and we suggest that each perspective has something to offer both society and the science of ecology. We present s...

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. <20% 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.

Extra-pair paternity and the evolution of testis size in a behaviorally monogamous tropical mammal, the large treeshrew (Tupaia tana)

Monogamy is rare in mammals (<5% spp.) but occurs in greater frequency among primates (15%) and their close relatives, the treeshrews (100%; Order: Scandentia). Two genetic studies of parentage in monogamous primates revealed high rates of extra-pair paternity (EPP), but to date parentage has not been studied in a treeshrew species. I analyzed the genetic parentage of 22 offspring from two populations of large treeshrews in Sabah, Malaysia (NE Borneo), using seven autosomal microsatellite loci and one mitochondrial DNA marker. Half of these offspring were sired by males that were not the presumed partner of the mother (50% EPP), and three litters exhibited evidence of multiple paternity. However, comparative analysis indicated that the high rate of EPP in Tupaia tana is not associated with intense sperm competition. Relative testis size of treeshrews was similar to testis size in 22 primate species with uni-male mating systems but smaller than 44 primates with multi-male mating systems. After factoring out the effects of body size and phylogeny, I also found that the evolution of multi-male mating systems was significantly associated with the evolution of larger testis size. Male–female pairs of T. tana occupy joint territories but forage and sleep alone (“dispersed pair-living”), and I argue that this form of behavioral monogamy renders mate guarding ineffective. The adaptive advantages of behavioral monogamy likely differ from the advantages driving EPP in large treeshrews. However, small testis size suggests that behavioral monogamy is not masking a dispersed multi-male mating system in this species.

DIET INFLUENCES LIFE SPAN IN PARROTS (PSITTACIFORMES)

Abstract Evolutionary hypotheses regarding longevity predict that life span should increase as extrinsic mortality rates decrease. Specifically, a decline in age-specific survival and fertility should evolve and decrease life span in proportion to the magnitude of the mortality risk. We examined these ideas using a new data set on maximum longevity, ecology, and life history of 162 parrot species (Psittaciformes). Parrots are generally long-lived but exhibit remarkable variation in life span between similar-sized genera, with particularly long-lived species occurring in the Cacatua, Calyptorhynchus, and Amazona. After controlling for both body size and phylogenetic ancestry using a phylogenetic supertree of all 352 parrot species, type of diet and communal roosting explain significant variation in parrot life span, but the influence of communal roosting is statistically dependent on an association with diet type. We suggest that extreme longevity in parrots has evolved in response to species-specific characteristics of diet, habitat, and behavior that influence extrinsic mortality rates. La Dieta Influencia la Longevidad en los Psittaciformes