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Rapid change in mouse mitochondrial DNA
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Wild mice around Chicago may have switched genotype to keep pace with modern living.
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... This study, although carried out in a confined geographical area (Britain), has shown that it is possible to detect true population replacements and distinguish them from selective sweeps at one or a few loci by using large SNP datasets in elaborate tests of population scenarios. Although mtDNA turnovers have been shown to have occurred in other species elsewhere and at various times in the past (Barnes et al., 2002;Pergams et al., 2003;Dalén et al., 2012), the colonization of Britain by bank voles (and other small mammals) is one of the best-studied models of mtDNA replacement in association with recolonization at the Pleistocene-Holocene transition. ...
The legacy of climatic changes during the Pleistocene glaciations allows inferences to be made about the patterns and processes associated with range expansion/colonization, including evolutionary adaptation. With the increasing availability of population genomic data, we have the opportunity to examine these questions in detail and in a variety of non-traditional model species. As an exemplar, here we review more than two decades of work by our group and others that illustrate the potential of a single “non-model model” mammal species - the bank vole (Clethrionomys glareolus), which is particularly well suited to illustrate the complexities that may be associated with range expansion and the power of genomics (and other datasets) to uncover them. We first summarize early phylogeographic work using mitochondrial DNA and then describe new phylogeographic insights gained from population genomic analysis of genome-wide SNP data to highlight the bank vole as one of the most compelling examples of a forest mammal, that survived in cryptic extra-Mediterranean (“northern”) glacial refugia in Europe, and as one of the species in which substantial replacement and mixing of lineages originating from different refugia occurred during end-glacial colonization. Our studies of bank vole hemoglobin structure and function, as well as our recent ecological niche modeling study examining differences among bank vole lineages, led us to develop the idea of “adaptive phylogeography.” This is what we call the study of the role of adaptive differences among populations in shaping phylogeographic patterns. Adaptive phylogeography provides a link between past population history and adaptation that can ultimately help predict the potential of future species responses to climate change. Because the bank vole is part of a community of organisms whose range has repeatedly contracted and then expanded in the past, what we learn from the bank vole will be useful for our understanding of a broad range of species.
... Differences in the genetic diversity over time provides valuable information on whether modern genetic patterns are more heavily influenced by long-term processes such as climate change, or if the decline in genetic diversity is more recent, caused primarily by population fragmentation and population decline driven by human-associated factors (Pliocene musk ox Ovibos moschatus: Campos et al. 2010; late quaternary megafauna: Lorenzen et al. 2011; Hawaiian Petrel Pterodroma sandwichensis: Welch et al. 2012; Ethiopian wolf Canis simensis: Gottelli et al. 2013; Kea Nestor notabilis: Dussex et al. 2015). Some studies have shown no change in phylogeographic patterns across temporal scales (kangaroo rat Dipodomys panamintinus: Thomas et al. 1990; red fox Vulpes vulpes: Teacher et al. 2011), while others show significant shifts in the distribution of genetic diversity over relatively short time-scales (brown bear Ursus arctos: Leonard et al. 2000; tiger beetle Coleoptera, Cicindelidae: Goldstein and Desalle 2003; mice Peromyscus leucopus noveboracensis: Pergams et al. 2003; hawk moth Hyles euphorbiae: Mende and Hundsdoerfer 2013). The South African endemic Cape Parrot Poicephalus robustus Gmelin 1788 provides a suitable model system for studying the relative impact of long-term climate change versus the more recent impact of anthropogenic factors on genetic variation. ...
The Cape Parrot Poicephalus robustus is a habitat specialist, restricted to forest patches in the Eastern Cape (EC), KwaZulu-Natal (KZN) and Limpopo provinces of South Africa. Recent census estimates suggest that there are less than 1,600 parrots left in the wild, although historical data suggest that the species was once more numerous. Fragmentation of the forest biome is strongly linked to climate change and exploitation of the forest by the timber industry. We examine the subpopulation structure and connectivity between fragmented populations across the distribution of the species. Differences in historical and contemporary genetic structure of Cape Parrots is examined by including both modern samples, collected from 1951 to 2014, and historical samples, collected from 1870 to 1946. A total of 114 individuals (historical = 29; contemporary = 85) were genotyped using 16 microsatellite loci. We tested for evidence of partitioning of genotypes at both a temporal and spatial scales by comparing shifts in allelic frequencies of historical (1870–1946) and contemporary (1951–2014) samples across the distribution of the species. Tests for population bottlenecks were also conducted to determine if anthropogenic causes are the main driver of population decline in this species. Analyses identified three geographically correlated genetic clusters. A southern group restricted to forest patches in the EC, a central group including birds from KZN and a genetically distinct northern Limpopo cluster. Results suggest that Cape Parrots have experienced at least two population bottlenecks. An ancient decline during the mid-Holocene (∼ 1,800-3,000 years before present) linked to climate change, and a more recent bottleneck, associated with logging of forests during the early 1900s. This study highlights the effects of climate change and human activities on an endangered species associated with the naturally fragmented forests of eastern South Africa. These results will aid conservation authorities with the planning and implementation of future conservation initiatives. In particular, this study emphasises the Eastern Cape mistbelt forests as an important source population for the species and calls for stronger conservation of forest patches in South Africa to promote connectivity of forest taxa.
... Recent studies have also utilized historical mammal specimens to screen for diseases that have potentially led to local extinction or population decline (Wyatt et al. 2008;Ávila-Arcos et al. 2013;Campana et al. 2017). Others have examined population changes over the last century in carnivores (Pertoldi et al. 2001;Larson et al. 2002;Wisely et al. 2002;Flagstad et al. 2003;Nyström et al. 2006;Hofman et al. 2015), bovids , and rodents (Thomas et al. 1990;Hadly et al. 1998;Hale et al. 2001;Pergams et al. 2003;Bi et al. 2013). Of particular interest is the ability to generate multilocus nuclear data sets from historical mammal specimens using hybridization capture techniques (Hawkins et al. 2016), including thousands of nuclear loci, which have allowed for historical population genomics for century-old specimens (Bi et al. 2013). ...
High-throughput sequencing methods have facilitated obtaining large amounts of data from degraded DNA, thus resulting in a dramatic increase in destructive sampling requests to museums. Because the tissues taken from museum specimens as sources of DNA are destroyed during analysis, consideration of the costs and benefits of loss of valuable specimen material relative to knowledge gained is required for any project utilizing destructive sampling. Variation exists in the preservation of DNA in historical specimens due to specimen age and type of museum preparation, among other factors. Thus, it is important to assess DNA yield and quality from different sources of museum specimens when considering the needs of a particular molecular project. We compared DNA derived from several common sources of museum specimens including bone, claw, skin, and soft tissue adherent to skeletal preparations. To account for differences in preparation type and therefore specimen preservation, we tested the performance of samples representing 3 taxonomic groups: mephitids, rodents, and marsupials. We also compared yields from 2 commonly used DNA extraction techniques. DNA quality was assessed by comparing average fragment size, concentration, and copy number of template DNA (for mitochondrial and nuclear markers) in genomic DNA extracts, as well as mitochondrial genome sequence coverage resulting from shotgun sequencing. We show that DNA quality derived from historic museum samples differs depending on specimen and sample type; however, all samples yielded high mitochondrial copy number except the skin and nail from the tanned specimen. Overall, claw samples produced the greatest number of high-quality sequencing reads with the least amount of bacterial contamination. We also found that high DNA concentrations did not necessarily result in high percentages of on-target reads; in fact, the samples that yielded the highest DNA quantities also had the highest amount of exogenous bacterial DNA. Our results indicate that most historical tissue types can be suitable for next-generation sequencing approaches, therefore providing multiple options for natural history collection staff and researchers when considering destructive sampling requests.
... Recent studies have also utilized historical mammal specimens to screen for diseases that have potentially led to local extinction or population decline (Wyatt et al. 2008;Ávila-Arcos et al. 2013;Campana et al. 2017). Others have examined population changes over the last century in carnivores (Pertoldi et al. 2001;Larson et al. 2002;Wisely et al. 2002;Flagstad et al. 2003;Nyström et al. 2006;Hofman et al. 2015), bovids , and rodents (Thomas et al. 1990;Hadly et al. 1998;Hale et al. 2001;Pergams et al. 2003;Bi et al. 2013). Of particular interest is the ability to generate multilocus nuclear data sets from historical mammal specimens using hybridization capture techniques (Hawkins et al. 2016), including thousands of nuclear loci, which have allowed for historical population genomics for century-old specimens (Bi et al. 2013). ...
High-throughput sequencing methods have facilitated obtaining large amounts of data from degraded DNA, thus resulting in a dramatic increase in destructive sampling requests to museums. Because the tissues taken from museum specimens as sources of DNA are destroyed during analysis, consideration of the costs and benefits of loss of valuable specimen material relative to knowledge gained is required for any project utilizing destructive sampling. Variation exists in the preservation of DNA in historical specimens due to specimen age and type of museum preparation, among other factors. Thus, it is important to assess DNA yield and quality from different sources of museum specimens when considering the needs of a particular molecular project. We compared DNA derived from several common sources of museum specimens including bone, claw, skin, and soft tissue adherent to skeletal preparations. To account for differences in preparation type and therefore specimen preservation, we tested the performance of samples representing 3 taxonomic groups: mephitids, rodents, and marsupials. We also compared yields from 2 commonly used DNA extraction techniques. DNA quality was assessed by comparing average fragment size, concentration, and copy number of template DNA (for mitochondrial and nuclear markers) in genomic DNA extracts, as well as mitochondrial genome sequence coverage resulting from shotgun sequencing. We show that DNA quality derived from historic museum samples differs depending on specimen and sample type; however, all samples yielded high mitochondrial copy number except the skin and nail from the tanned specimen. Overall, claw samples produced the greatest number of high-quality sequencing reads with the least amount of bacterial contamination. We also found that high DNA concentrations did not necessarily result in high percentages of on-target reads; in fact, the samples that yielded the highest DNA quantities also had the highest amount of exogenous bacterial DNA. Our results indicate that most historical tissue types can be suitable for next-generation sequencing approaches, therefore providing multiple options for natural history collection staff and researchers when considering destructive sampling requests.
... However, recent findings on mitochondrial DNA (mtDNA) of British small mammals [4,5,7] revealed a genetic turnover in southern Britain during the Pleistocene-Holocene transition where one mtDNA clade of each species was replaced with another mtDNA clade of the same species. Although mtDNA turnovers have been inferred for other species elsewhere and at various times in the past [8][9][10], the colonization of Britain by small mammals is now one of the best-studied models of mtDNA replacement in association with recolonization at the Pleistocene-Holocene transition [4,5,11]. ...
Current species’ distributions at high latitudes are the product of expansion from glacial refugia into previously uninhabitable areas at the end of the last glaciation. The traditional view of postglacial colonization is that southern populations expanded their ranges into unoccupied northern territories. Recent findings on mitochondrial DNA (mtDNA) of British small mammals have challenged this simple colonization scenario by demonstrating a more complex genetic turnover in Britain during the Pleistocene-Holocene transition where one mtDNA clade of each species was replaced by another mtDNA clade of the same species. Here, we provide evidence for one of those small mammals, the bank vole (Clethrionomys glareolus), that the replacement was genome-wide. Using more than 10,000 autosomal SNPs we found that similar to mtDNA, bank vole genomes in Britain form two (north and south) clusters which admix. Therefore, the genome of the original post-glacial colonists (the northern cluster) was likely replaced by another wave of migration from a different continental European population (the southern cluster), and we gained support for this by modelling with approximate Bayesian computation. This finding emphasises the importance of analysis of genome-wide diversity within species under changing climate in creating opportunities for sophisticated testing of population history scenarios.
... It is unclear how molecular evolution proceeds in specified environments. It is unclear how commensal relationships affect their molecular characteristics (Pergams et al. 2003). It is unclear how much rate variation occurs. ...
... These findings that NYC populations are genetically isolated but still maintain high levels of neutral genetic variation [36][37][38] indicated that the conditions for local adaptation to urban conditions may be widespread for white-footed mice and other urban Peromyscus [39]. Indeed, temporal replacement of mitochondrial haplotypes had previously been reported for Chicago-area P. leucopus, suggesting rapid evolution in urban populations [40,41]. ...
Deer mice in the genus Peromyscus occupy nearly every terrestrial habitat in North America, and have a long history as subjects of behavioral, ecological, evolutionary, and physiological study. Recent advances in transcriptomics, the study of the complete set of RNA transcripts produced by certain cell types or under certain conditions, have contributed to the development of Peromyscus as a model system. We review the recent use of transcriptomics to investigate how natural selection and gene expression plasticity contribute to the existence of deer mice in challenging environments such as highlands, deserts, and cities across North America. Transcriptomics also holds great promise for elucidating the genetic basis of mating systems and other behaviors in Peromyscus, but has to date been underutilized for developmental biology and disease studies. Future Peromyscus studies should apply robust comparative frameworks to analyze the transcriptomics of multiple populations of the same species across varying environmental conditions, as well as multiple species that vary in traits of interest.
... Habitat fragmentation in landscapes have effects on species' genetic variation and population demography (Gaines et al., 1997;Bender et al., 1998;Gibbs, 2001;Pergams et al., 2003). Dongting Lake has been changing since the Pleistocene. ...
To understand genetic variation and population dispersal in the Yangtze vole Microtus fortis calamorum distributed in the Dongting Lake region, 144 individuals were collected from six habitat patches. The mitochondrial DNA control region was sequenced and 17 haplotypes were observed. Of the six investigated populations, haplotype and nucleotide diversities of those from larger patches were higher than those from smaller patches. Nonparametric correlation analysis showed that patch size had a positive correlation with haplotype diversity (r = 0.943, P < 0.01). A neighbour-joining tree of the 17 haplotypes showed no geographic genetic structure among the six populations. Analysis of isolation by distance showed that genetic differentiation among the six populations was not positively related to geographic distance. Analysis of mismatch distribution indicated that the voles had passed through a population expansion. The pattern of haplotype distribution in the Changsha population suggests that the population was established by a founder effect [Current Zoology 58 (2): 211–220, 2012].
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.
Genetic studies have shown that New York City white-footed mouse (Peromyscus leucopus) populations 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 genetic 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 morphological 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 chewing 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.
The prairie deer mouse (Peromyscus maniculatus bairdii ) was more common than the white-footed mouse (P. leucopus) in museum collections from the 6 Illinois counties of the Chicago region before 1920 but constitutes only 5% of specimens deposited since 1970. Because white-footed mouse prefers woody vegetation and because prairie deer mouse is limited to prairie or large open habitats, the change in proportion is likely driven by a disproportionate loss of prairie among remaining natural habitat and increases in woody vegetation within grasslands. The decline of the prairie vole ( Microtus ochrogaster) relative to the meadow vole (M. pennsylvanicus) and the lack of recent specimens of Franklin's ground squirrel (Spermophilus franklinii) corroborate the hypothesis that prairie habitats have declined much more so than wooded habitats in the Chicago region. Based on ex- tinction models using museum records, it is probable that S. franklinii is already locally extirpated. Regression analysis suggests the white-footed mouse will be the only local Peromyscus in 0-140 years.
A target length limitation to PCR amplification of DNA has been identified and addressed. Concomitantly, the base-pair fidelity, the ability to use PCR products as primers, and the maximum yield of target fragment were increased. These improvements were achieved by the combination of a high level of an exonuclease-free, N-terminal deletion mutant of Taq DNA polymerase, Klentaq1, with a very low level of a thermostable DNA polymerase exhibiting a 3'-exonuclease activity (Pfu, Vent, or Deep Vent). At least 35 kb can be amplified to high yields from 1 ng of lambda DNA template.
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KlenTaq DNA polymerase is an N-terminally truncated Thermus aquaticus (Taq) DNA polymerase I. As expressed from a gene construct in Escherichia coli, translation initiates at Met236, bypassing the 5'----3' exonuclease domain of the DNA polymerase-encoding gene. A sensitive forward mutation assay was used to measure the relative number of mutations introduced into the entire lacZ gene by the polymerase chain reaction (PCR) under various conditions which allow the amplification of such a large DNA span. Two selectable markers, one at each end of the test lacZ fragment, were employed to avoid the plating and scoring of PCR artefacts such as primer initiation in the midst of the lacZ gene, and cloning artefacts such as empty vector plasmid. The measured relative mutation rate was twofold lower for KlenTaq as compared to the full-length Taq DNA polymerase.
Procedures utilizing Chelex 100 chelating resin have been developed for extracting DNA from forensic-type samples for use with the PCR. The procedures are simple, rapid, involve no organic solvents and do not require multiple tube transfers for most types of samples. The extraction of DNA from semen and very small bloodstains using Chelex 100 is as efficient or more efficient than using proteinase K and phenol-chloroform extraction. DNA extracted from bloodstains seems less prone to contain PCR inhibitors when prepared by this method. The Chelex method has been used with amplification and typing at the HLA DQ alpha locus to obtain the DQ alpha genotypes of many different types of samples, including whole blood, bloodstains, seminal stains, buccal swabs, hair and post-coital samples. The results of a concordance study are presented in which the DQ alpha genotypes of 84 samples prepared using Chelex or using conventional phenol-chloroform extraction are compared. The genotypes obtained using the two different extraction methods were identical for all samples tested.
A PCR method for uniform amplification of a mixture of DNA templates differing in GC content is described using the two enzyme approach (Klentaq1 and Pfu DNA polymerase) and a combination of DMSO and betaine. This method was applied to amplify the CGG repeat region from the fragile X region.
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