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Signatures of rapid evolution in urban and rural transcriptomes of white-footed mice (Peromyscus leucopus) in the New York metropolitan area.

Harris SE, Munshi-South J, Obergfell C, O'Neill R - PLoS ONE (2013)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Program in Ecology, Evolutionary Biology, & Behavior, The Graduate Center, City University of New York (CUNY), New York, New York, United States of America.

ABSTRACT
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, Peromyscusleucopus, 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.

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Related in: MedlinePlus

Non-synonymous (pN) SNP substitutions plotted vs. synonymous (pS) substitutions for 354 genes.Each circle represents one unique assembled contig. (a) Pairwise comparisons for all urban populations. (b) Pairwise comparisons for urban to rural populations. The dashed line denotes pN / pS = 1, and circles above the line (pN / pS > 1) indicate candidates for positive selection. The solid line shows the slope for pN / pS = 0.5.
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pone-0074938-g005: Non-synonymous (pN) SNP substitutions plotted vs. synonymous (pS) substitutions for 354 genes.Each circle represents one unique assembled contig. (a) Pairwise comparisons for all urban populations. (b) Pairwise comparisons for urban to rural populations. The dashed line denotes pN / pS = 1, and circles above the line (pN / pS > 1) indicate candidates for positive selection. The solid line shows the slope for pN / pS = 0.5.

Mentions: After mapping the reads used in the assembly back to the Newbler cDNA reference transcriptome, 31,015 SNPs were called in 7,625 isotigs. The distribution of SNPs per isotig ranged from 1-78 (mean = 4 ± 5.4; median = 2). ORFs were identified in 11,704 isotigs comprising 5.6 Mb of sequence, and 2,655 putative ORFs contained 4,893 SNPs. Of these SNPs, 1,795 (36.6%) were classified as non-synonymous and 3,098 (63.3%) were classified as synonymous. Aligned ORFs were used to calculate pN ⁄ pS between each pair of populations. The majority of the ORFs did not exhibit statistical signatures of positive selection (overall mean ± SE pN ⁄ pS = 0.28 ± 0.56). For the 2,307 pairs of homologous cDNA sequences between populations that contained predicted ORFs, did not contain in-frame stop codons, and had greater than or equal to three SNPs, pN ⁄ pS values for 11 (0.5%) contigs exceeded 1.0 (Table 4, Figure 5). The proportion of genes with pN ⁄ pS > 1.0 is comparable to similar studies; Sun et al. [23] found that 0.4% of genes in their Pomaceacanaliculata dataset were positively selected, Renaut et al. [54] reported 0.5% in Coregonusclupeaformis, and Wang et al [55] reported 1.8% in Bemisiatabaci. Four contigs (0.2%) exhibited pN ⁄ pS values > 1.0 in urban to urban comparisons and 7 contigs (0.3%) in urban to rural population comparisons. 42 (1.8%) contigs were found with pN ⁄ pS between 0.5 and 1 (Table S3, Figure 5); pN ⁄ pS greater than 0.5 is a less conservative filter for detecting positive selection, especially when using truncated ORFs [56,57].


Signatures of rapid evolution in urban and rural transcriptomes of white-footed mice (Peromyscus leucopus) in the New York metropolitan area.

Harris SE, Munshi-South J, Obergfell C, O'Neill R - PLoS ONE (2013)

Non-synonymous (pN) SNP substitutions plotted vs. synonymous (pS) substitutions for 354 genes.Each circle represents one unique assembled contig. (a) Pairwise comparisons for all urban populations. (b) Pairwise comparisons for urban to rural populations. The dashed line denotes pN / pS = 1, and circles above the line (pN / pS > 1) indicate candidates for positive selection. The solid line shows the slope for pN / pS = 0.5.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3756007&req=5

pone-0074938-g005: Non-synonymous (pN) SNP substitutions plotted vs. synonymous (pS) substitutions for 354 genes.Each circle represents one unique assembled contig. (a) Pairwise comparisons for all urban populations. (b) Pairwise comparisons for urban to rural populations. The dashed line denotes pN / pS = 1, and circles above the line (pN / pS > 1) indicate candidates for positive selection. The solid line shows the slope for pN / pS = 0.5.
Mentions: After mapping the reads used in the assembly back to the Newbler cDNA reference transcriptome, 31,015 SNPs were called in 7,625 isotigs. The distribution of SNPs per isotig ranged from 1-78 (mean = 4 ± 5.4; median = 2). ORFs were identified in 11,704 isotigs comprising 5.6 Mb of sequence, and 2,655 putative ORFs contained 4,893 SNPs. Of these SNPs, 1,795 (36.6%) were classified as non-synonymous and 3,098 (63.3%) were classified as synonymous. Aligned ORFs were used to calculate pN ⁄ pS between each pair of populations. The majority of the ORFs did not exhibit statistical signatures of positive selection (overall mean ± SE pN ⁄ pS = 0.28 ± 0.56). For the 2,307 pairs of homologous cDNA sequences between populations that contained predicted ORFs, did not contain in-frame stop codons, and had greater than or equal to three SNPs, pN ⁄ pS values for 11 (0.5%) contigs exceeded 1.0 (Table 4, Figure 5). The proportion of genes with pN ⁄ pS > 1.0 is comparable to similar studies; Sun et al. [23] found that 0.4% of genes in their Pomaceacanaliculata dataset were positively selected, Renaut et al. [54] reported 0.5% in Coregonusclupeaformis, and Wang et al [55] reported 1.8% in Bemisiatabaci. Four contigs (0.2%) exhibited pN ⁄ pS values > 1.0 in urban to urban comparisons and 7 contigs (0.3%) in urban to rural population comparisons. 42 (1.8%) contigs were found with pN ⁄ pS between 0.5 and 1 (Table S3, Figure 5); pN ⁄ pS greater than 0.5 is a less conservative filter for detecting positive selection, especially when using truncated ORFs [56,57].

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Program in Ecology, Evolutionary Biology, & Behavior, The Graduate Center, City University of New York (CUNY), New York, New York, United States of America.

ABSTRACT
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, Peromyscusleucopus, 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.

Show MeSH
Related in: MedlinePlus