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Morphological Differentiation in White-Footed Mouse (Mammalia: Rodentia: Cricetidae: Peromyscus Leucopus

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Morphological Differentiation in White-Footed Mouse (Mammalia: Rodentia: Cricetidae: Peromyscus Leucopus See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/316142754 Morphological Differentiation in White-footed Mouse (Mammalia: Rodentia: Cricetidae: Peromyscus leucopus... Article in Bulletin of the Peabody Museum of Natural History · April 2017 DOI: 10.3374/014.058.0102 CITATIONS READS 0 21 3 authors, including: Eric J. Sargis Yale University 121 PUBLICATIONS 2,000 CITATIONS SEE PROFILE Some of the authors of this publication are also working on these related projects: Paleocene–Eocene plesiadapiforms and Primate Origins View project Systematics and conservation of Rungwecebus kipunji (Primates, Cercopithecidae) View project All content following this page was uploaded by Eric J. Sargis on 15 April 2017. The user has requested enhancement of the downloaded file. All in-text references underlined in blue are added to the original document and are linked to publications on ResearchGate, letting you access and read them immediately. 01_Yu-etal_170001.qxd 4/5/17 12:41 PM Page 3 Morphological Differentiation in White-footed Mouse (Mammalia: Rodentia: Cricetidae: Peromyscus leucopus) Populations from the New York City Metropolitan Area Aimy Yu1, Jason Munshi-South2 and Eric J. Sargis3 1 Corresponding author: Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT USA —email: [email protected] 2 Department of Biological Sciences, Fordham University, Bronx, NY USA, and Louis Calder Center-Biological Field Station, Fordham University, Armonk, NY USA 3 Department of Anthropology, Yale University, and Division of Vertebrate Zoology, Yale Peabody Museum of Natural History, New Haven, CT USA Supplementary materials for this article are available online. ABSTRACT Genetic studies have shown that New York City white-footed mouse (Peromyscus leucopus) pop- ulations exhibit substantial genetic structure and high levels of allelic diversity and heterozygos- ity. These studies have also identified mutations and genes involved in the divergence of urban and rural P. leucopus populations. To investigate whether morphological change mirrors the ge- netic differentiation observed in New York City P. leucopus populations, we conducted univariate and multivariate analyses on 4 external and 14 skull variables to compare urban, suburban and rural P. leucopus populations from in and around New York City. The only significant morpho- logical differences among the three populations were in upper and lower toothrow lengths, both of which had high loadings in our principal components analyses. In general, rural individuals were found to have longer upper and lower toothrows than urban ones. This difference is likely due to the relationship between food quality and size of dental occlusal surfaces. Generally, lower- quality food requires more chewing and its consumption is facilitated by larger occlusal surfaces. Our results suggest that urban mice consume a higher-quality diet or food that requires less chew- ing than their rural counterparts by making use of the availability of natural food sources in rich, vegetative understories characteristic of urban forest fragments. Our cluster analysis of the skull variables revealed that urban and suburban populations are more similar to one another than to the rural population. KEYWORDS Anthropogenic selection, evolution, mammals, morphology, morphometrics, urban ecology, urbanization Introduction of the world population is predicted to reside in urban areas by 2050 (United Nations 2015). Through industry, pollution and the introduc- Understanding how natural populations respond tion of invasive species, humans are responsible to human-dominated landscapes is thus increas- for rapid and pervasive alteration of the global ingly important. Urban systems deviate from landscape. Nowhere are humans more influen- rural systems and are characterized by distinct tial than in urban contexts. Humans sculpt the chemical and physical milieus, dynamic processes urban landscape and oversee many of its ecolog- and biotic communities. Multiple studies have ical processes, directly influencing the ways shown that cities are viable ecosystems in which organisms interact with each other and the envi- many organisms flourish (Faeth et al. 2005; ronment. More than half of the world’s popula- McKinney 2008). Ecologists and evolutionary tion now occupies urban areas and two-thirds biologists are interested in the ability of species Bulletin of the Peabody Museum of Natural History 58(1):3–16, April 2017. © 2017 Peabody Museum of Natural History, Yale University. All rights reserved. • http://peabody.yale.edu 01_Yu-etal_170001.qxd 4/5/17 12:41 PM Page 4 4 Bulletin of the Peabody Museum of Natural History 58(1) • April 2017 to adapt to these human-dominated ecosystems population size and density in the United States. (Donihue and Lambert 2015). Despite the large concentration of people, urban In the face of substantial ecological change, forests and vegetation make up a fifth of the city’s organisms can adapt (through evolution or phe- land cover (Lu et al. 2009; US Census Bureau notypic plasticity), migrate or go extinct. Urban- 2015). P. leucopus inhabits most surveyed, forested ization typically results in a considerable loss of areas in NYC, but is replaced by house mice (Mus biodiversity through habitat loss and fragmenta- musculus) and Norway rats in urban matrix dom- tion and the introduction of nonnative species. inated by impervious surfaces (J. Munshi-South, The destruction and transformation of large con- unpubl. data). In contrast to previous results from tinuous natural habitats into small isolated frag- nonurban Peromyscus populations, P. leucopus mented patches of urban habitats (e.g., city parks) populations in NYC’s forest fragments have high surrounded by barriers to dispersal (e.g., roads levels of allelic diversity and heterozygosity at neu- and buildings) reduces the number of “urban tral loci within populations (Munshi-South and avoiders,” which require large undisturbed con- Kharchenko 2010; Munshi-South et al. 2016). In tiguous habitats to sustain stable populations a related study, Munshi-South (2012) found that (Blair 2001; McKinney 2002, 2006). At the same gene flow among populations occurred through time that urban avoiders disappear, “urban vegetated corridors such as cemetery perimeters, exploiters” and “urban adapters” rise in numbers. unmowed fencerows and parkway medians. Mun- Urban exploiters are primarily nonnative species shi-South and Nagy (2014) reported that even that take advantage of ecological subsidies from small (as determined by park area) and very iso- humans (Johnston 2001). Commensal organisms lated (as determined by the number of years since such as pigeons and rats are examples of urban each park was founded and the number of years exploiters. Urban adapters are native species that since major infrastructure projects were completed can adapt to urban habitats and use both natural around park perimeters) patches of green spaces and urban resources (McKinney 2002, 2006). The are adequate to maintain genetic variation because pattern in which native biotas in urban areas are the observed heterozygosity of populations in replaced by nonnative commensals and locally larger urban parks, or parks that have been isolated expanding species is observed all over the world for shorter periods, was not greater than that of and is referred to as biotic homogenization (McK- populations in smaller more isolated urban parks. inney 2006). Harris et al. (2015) identified mutations and genes Urban adapters are of great interest for study- involved in the divergence of urban and rural ing the evolutionary consequences of urbaniza- P. leucopus populations by sequencing pooled tion in local populations. In particular, the mRNA. These genes play roles in xenobiotic white-footed mouse, Peromyscus leucopus, is an metabolism and immunological function. emerging model organism for such studies. This In response to environmental stresses associ- North American species is broadly distributed ated with urbanization, white-footed mouse pop- with a range covering the eastern two-thirds of the ulations evolved adaptations that better enabled United States and abutting portions of southern them to deal with new predators, competitors, Canada, extending into southern Mexico (Linzey pathogens, parasites, toxins and pollutants. et al. 2008). However, it is absent from the coastal Munshi-South et al. (2016) found that genomic plain areas of the southeastern states and Florida variation is inversely related to urbanization (as (Linzey et al. 2008). It occupies a variety of habi- measured by the percentage of impervious surface tats throughout its sizeable range, from semi- and human population density; see Materials and deserts to high-elevation forests, achieving highest Methods) and that urbanization increases genetic densities in warm, dry forests and brushy areas at differentiation among city populations. Using low to middle elevations (Linzey et al. 2008). At population genomic modeling, Harris et al. (2016) present, it is the only Peromyscus species in were able to distinguish recent anthropogenic the New York City (NYC) metropolitan area changes from older climatic events. They also (J. Munshi-South, unpubl. data). found that the estimated divergence times for sev- New York City, among the oldest and most eral recently isolated P. leucopus populations reflect developed cities in North America, has the largest the history of urbanization
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