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California Island deer mice: genetics, morphometrics, and evolution
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Deer mice, Peromyscus maniculatus, are found on all eight California Channel Islands and are classified as separate subspecies on each island. Distinct mitochondrial DNA haplotypes, identified by restriction enzyme analysis, were found in island deer mice, and on five of the eight islands deer mice have unique haplotypes, suggesting genetic isolation and independent evolution of several island subspecies. Founder effects on mtDNA diversity in island populations relative to mainland populations are evident. The connec-tivity of the deer mouse populations on East, Middle, and West Anacapa Islands (P. m. anacapae) was assessed using sequence data from the mitochondrial cytochrome c oxidase subunit II gene (COII). A common haplotype was found on all three Anacapa Islets, although Middle and East Anacapa each had an additional unique haplotype. This suggests that deer mice on Anacapa are functioning as a metapopulation, with some gene flow or extinction/recolonization occurring among the islets. Discriminant function analysis of cranial and external morphological characters for three island sub-species, P. m. anacapae, P. m. santacruzae, and P. m. elusus, produced a high rate of correct classification, indicating strong morphological as well as genetic differentiation. The specimens used for the morphometric study were museum specimens collected at different times during the past century. A surprising result of the morphological analysis was that each subspecies had exhibited extremely rapid change in several characters over this time period.
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... We should note that a preponderance of Cricetidae and Muridae exists in museum collections overall: for example 67.5% of all Rodentia specimens at the National Museum are Cricetidae and Muridae. Data from Channel Island deer mice[6,[27][28]and Chicago-area white-footed mice[11]were included. By continent, 13 cases were from North America (US, including Alaska), 11 from South America (Chile, Mexico, and Peru), three from Africa (Kenya), and one from Asia (Philippines). ...
In general, rapid morphological change in mammals has been infrequently documented. Examples that do exist are almost exclusively of rodents on islands. Such changes are usually attributed to selective release or founder events related to restricted gene flow in island settings. Here we document rapid morphological changes in rodents in 20 of 28 museum series collected on four continents, including 15 of 23 mainland sites. Approximately 17,000 measurements were taken of 1302 rodents. Trends included both increases and decreases in the 15 morphological traits measured, but slightly more trends were towards larger size. Generalized linear models indicated that changes in several of the individual morphological traits were associated with changes in human population density, current temperature gradients, and/or trends in temperature and precipitation. When we restricted these analyses to samples taken in the US (where data on human population trends were presumed to be more accurate), we found changes in two additional traits to be positively correlated with changes in human population density. Principle component analysis revealed general trends in cranial and external size, but these general trends were uncorrelated with climate or human population density. Our results indicate that over the last 100+ years, rapid morphological change in rodents has occurred quite frequently, and that these changes have taken place on the mainland as well as on islands. Our results also suggest that these changes may be driven, at least in part, by human population growth and climate change.
... It is commonly observed that insular rodents differ from their mainland relatives in a variety of traits, including behaviour, demography, genetics, physiology, and morphology (Gliwicz 1980;Berry 1986;Adler & Levins 1994;Abdelkrim et al. 2005). Recent work has further confirmed the generality of increased rates of morphological evolution in island mammals (Millien 2006).Pergams & Ashley (2001)performed a meta-analysis of rapid morphological evolution in island rodents: in Mus musculus after introduction to islands of the North Atlantic; in Rattus rattus after introduction to the Galapagos Islands; and in Peromyscus maniculatus on the California Channel Islands (Pergams & Ashley 2000). The authors found that microevolution of body size and skeletal traits are greater on smaller and more remote islands. ...
We report rapid change of morphology and mitochondrial genes in white-footed mice (Peromyscus leucopus) in the Chicago (Illinois, USA) region. We sequenced mitochondrial DNA COX2 from 55 museum skins of white-footed mice caught in the Chicago area since 1855 and from 44 mice recently trapped in the same locations. We found consistent directional genotype replacement at five separate collection locations. We later focused on a single one of these locations (Volo Bog State Natural Area) and sequenced mitochondrial D-loop control region from 58 museum skins of mice collected in 1903-1976 and 32 mice recently trapped there. We found complete and more recent replacement of D-loop haplotypes, apparently occurring between 1976 and 2001. We tested whether these genetic changes were mirrored by changes in morphology by comparing 15 external and cranial traits. We found no significant morphological differences between mice collected in 1903-1976; however, mice collected in 2001-2003 showed 9 of 15 measurements to be significantly changed relative to the earlier samples. Recent mice were longer in total length, with broader, longer noses, and longer but shallower skulls(1). Discriminant function analysis allowed for 100% correct classification using these traits. Principal components analysis shows variance over time is well distributed across both external and cranial measures. The sequential replacements of haplotypes and the rapid change of morphology can best be explained by replacement of the regional population with immigrants from genetically distinct neighbouring populations, likely facilitated by the large environmental changes occurring over the time period. Replacement with genotypes from external populations may be a common mechanism of evolution of newly adaptive local forms in an increasingly human-impacted world.
Rats and mice are among the most successful mammals on earth, with some of these species thriving in and around human settlements or areas disturbed by human activities. Here, we present morphological, taphonomic, and chronological data on two mice (Peromyscus nesodytes [extinct] and P. maniculatus [extant]) from a trans-Holocene sequence at Daisy Cave, San Miguel Island, California. We explore the colonization history of each species, species abundance through time, taphonomic history, and the causes and timing of the extinction of P. nesodytes. P. maniculatus were probably introduced by humans to San Miguel Island ~11,000 years ago, 1000 years earlier than previous estimates, and P. nesodytes does not occur in Daisy Cave deposits after ~8000 years ago, some 7000 years earlier than reported at adjacent Cave of the Chimneys. Island P. maniculatus form a distinct morphological group from all other North American subspecies. These data highlight the importance of morphological analyses of archaeological and subfossil rodent specimens for understanding the evolution and natural history of island endemic species and their interactions with humans.
Rapid morphological change has been shown in rodent populations on islands, including endemic deer mice (Peromyscus maniculatus subspp.) on the California Channel Islands. Surprisingly, most of these changes were towards a smaller size. Black rats were introduced to Anacapa Island in the mid-1800s (probably in 1853) and eradicated in 2001–2002. To assess possible changes in these rats since their introduction, eleven cranial and four standard external measurements were taken from 59 Rattus rattus specimens collected from 1940–2000. All rat cranial traits changed 3.06–10.43% (724–2567 d, 0.06–0.42 h), and all became larger. When considered in haldanes, these changes are among the fastest on record in any organism, and far exceed changes found in other island rodents. These changes were confirmed by MANOVA (Wilk’s
λ < 0.0005, Fd.f.15 = 2974.386, P < 0.0005), and all 11 cranial traits significantly fit linear regressions. We speculate that concurrent changes in mice may have been due in part to competition with and/or predation by rats. Future research might evaluate whether the vector of mouse evolution on Anacapa is again changing after rat eradication.
The island spotted skunk (Spilogale gracilis amphiala) is endemic to the 2 largest California Channel Islands, Santa Cruz and Santa Rosa. Unlike the island fox (Urocyon littoralis) and island subspecies of the deer mouse (Peromyscus maniculatus), the island spotted skunk shows no morphological differentiation between islands and is differentiated only weakly from mainland subspecies, suggesting recent colonization. However, the islands have been isolated from each other and the mainland throughout the Quaternary Period. We used 8 microsatellite loci to investigate the distribution of genetic variation within and among populations of spotted skunks from 8 localities (the 2 islands and 6 mainland localities), representing 4 subspecies. Tissue samples were obtained from 66 fresh specimens collected from 2000 to 2002 and 142 museum specimens collected from 1906 to 1994. Allelic richness and heterozygosity in island spotted skunk populations was approximately 30% lower than that found in mainland localities or subspecies. All localities or subspecies were significantly differentiated (mean F ST was 0.17 and 0.13 for localities and subspecies, respectively). Contrary to comparisons based on morphological data, genetic differentiation was especially strong between islands and between island and mainland localities or subspecies. Patterns of differentiation suggest that skunks colonized the Channel Islands shortly before rising sea levels separated Santa Cruz and Santa Rosa islands (11,500 years ago). Our results indicate that the taxonomic status of the island spotted skunk should be reconsidered and that both island populations might constitute evolutionarily significant units worthy of conservation.
Eradication of introduced predators has become an increasingly important restoration strategy on islands since the 1970s, but the benefits for impacted seabird populations are seldom examined. Scripps’s murrelet (Synthliboramphus scrippsi), a small crevice nesting alcid, suffered severe impacts from introduced mammals at all breeding islands through much of the 19th and 20th centuries. From 2001 to 2010, nest monitoring was conducted to assess responses of the remnant murrelet population at Anacapa Island, California after black rats (Rattus rattus) were eradicated in 2002. Baseline (2001–2002) and post-eradication (2003–2010) monitoring in ten sea caves recorded a nearly 3-fold increase in hatching success (30% versus 85%), due mainly to a drastic reduction in egg predation. Post-eradication monitoring in caves was augmented with three plots in previously vacant “non-cave” habitats that were occupied within 1–3 years of rat eradication. Nests increased 10% per annum in sea caves, 24% in non-cave plots and 14% overall. Murrelet nesting was limited mostly to remnant breeding habitats, consistent with recruitment of philopatric local cohorts as the major factor in colony growth. No nests were found during limited searches of suitable crevices on upper-island slopes and cliffs. Continued monitoring at Anacapa is needed to document the long-term progress and rate of colony recovery and detect nesting in currently vacant habitats. Better knowledge of the post-eradication responses of seabirds will assist development of more effective island restoration actions; thus, baseline and post-eradication monitoring should be essential components of more eradication programs in the future.
Microtus pennsylvanicus is represented in Mexico only by the Chihuahuan meadow vole (M. p. chihuahuensis), known from only 1 disjunct population in a small and isolated marsh in the arid lands of northern Chihuahua. Livetrapping conducted between 2000 and 2004 provided no specimens of M. p. chihuahuensis, nor was any sign of this vole observed. By the end of this study the marsh providing water had been drained, thereby destroying the vole's habitat. Surveys of other marshes in northern Chihuahua also failed to produce evidence of the species. We therefore conclude that M. p. chihuahuensis has been extirpated from its only known locality. Using "ancient" DNA from museum specimens we evaluated genetic divergence between museum specimens of M. p. chihuahuensis and 46 extant Microtus species and subspecies. Our results support the subspecific status of M. p. chihuahuensis. The loss of this subspecies is an example of population extinction, a very severe form of biodiversity loss. Until recently such losses have been mostly neglected.
Random amplified polymorphic DNA (RAPD) markers were used to estimate the level and pattern of genetic diversity in Microtus fortis pelliceus populations from the mainland and islands of the Russian Far East. No markers were found both for individual populations and for the mainland or island voles as a whole. However, they appeared to be different in both their allele frequencies and microevolution mode based on correlation pleiad analysis. The island populations demonstrated a higher level of genetic differentiation among themselves than did mainland populations and each mainland population probably represents more genetic diversity than any population of islands. Overall, genetic variation between island and mainland M. f. pelliceus populations was low (Dst = 0.003), and can be explained by a low value of gene differentiation coefficient (Gst = 0.058). Nevertheless, exact test did not support the hypothesis that both united mainland and united island populations belong to the same genetic unit (p = 0.0025). RAPD data reliably distinguished voles of Matveeva Island, which are strongly differentiated by morphological traits, and this in turn did not exclude the island speciation event. Unlike UPGMA and NJ trees for individuals, population UPGMA strongly separated island voles from the mainland conspecifics, and MS reconctructions identified the Amur population as an ancestor.
We perform a meta-analysis on morphological data from four island rodent populations exhibiting microevolution (>100 years). Data consisting of incidences of skeletal variants, cranial, and external measurements are from house mice (Mus musculus) on one Welsh and one Scottish island, black rats (Rattus rattus) on two Galapagos islands, and deer mice (Peromyscus maniculatus) on three California Channel islands. We report extremely high rates of microevolution for many traits; 60% of all mensural traits measured changed at a rate of 600 d or greater (max. 2682 d). The proportion of all mensural traits evolving at 600–800 d (23%) was idiosyncratic and departed from an expected negative exponential distribution. We argue that selection, rather than founder events, is largely responsible for the substantial shifts in morphology seen among insular rodents. Examining individual traits, there is a trend towards the nose becoming longer and wider, while the skull becomes shallower, shown by both rats and mice on five different islands. We found a significant correlation between island size and degree of skeletal variant evolution and between island distance from the mainland (or nearest island) and degree of cranial and external character evolution. Thus, microevolution of rodents is greater on smaller and more remote islands.
Relation entre la distance geographique et la phylogenese etudie chez des populations de la souris Peromyscus maniculatus des iles du detroit de Californie a l'aide de donnees morphologiques, biologiques et du RFLP de l'ADN mitochondrial
Deer mice, Peromyscus maniculatus, collected over 90 years from three California Channel Islands, were examined for evidence of morphological change. Rapid morphological change has occurred in the endemic subspecies from Santa Barbara (P. m. elusus), Anacapa (P. m. anacapae), and Santa Cruz Island (P. m. santacruzae). Data were divided into two temporal classes, 1897-1941 and 1955-1988. Of the 16 morphological characters measured, between five and 10 measures changed significantly (P ⩽ 0.05) with temporal class in each subspecies, and multivariate test statistics were significant (P ⩽ 0.05) for all three subspecies. For each subspecies, depth of braincase, total length, tail length, and hind foot length became smaller over time, except depth of braincase, which became larger in P. m. elusus. The rates of change dramatically exceed those estimated from paleontological records and are even higher than those reported in some experimental selection studies. Temporal change in two characters exceeds differentiation between subspecies. Although changing, each subspecies remained well differentiated, and incorporation of temporal change allowed correct classification of most specimens. Unlike nearly all previous reports of rapid evolution, the changes in these populations were not associated with a founder events or recent introductions. This study demonstrates that rapid phenotypic change can occur in long-established natural populations and temporal stability of morphological characters in such populations, even over short evolutionary time periods, cannot be assumed.
Data on DNA polymorphisms detected by restriction endonucleases are rapidly accumulating. With the aim of analyzing these data, several different measures of nucleon (DNA segment) diversity within and between populations are proposed, and statistical methods for estimating these quantities are developed. These statistical methods are applicable to both nuclear and non-nuclear DNAs. When evolutionary change of nucleons occurs mainly by mutation and genetic drift, all the measures can be expressed in terms of the product of mutation rate per nucleon and effective population size. A method for estimating nucleotide diversity from nucleon diversity is also presented under certain assumptions. It is shown that DNA divergence between two populations can be studied either by the average number of restriction site differences or by the average number of nucleotide differences. In either case, a large number of different restriction enzymes should be used for studying phylogenetic relationships among related organisms, since the effect of stochastic factors on these quantities is very large. The statistical methods developed have been applied to data of Shah and Langley on mitochondrial (mt)DNA from Drosophila melanogaster, simulans and virilis. This application has suggested that the evolutionary change of mtDNA in higher animals occurs mainly by nucleotide substitution rather than by deletion and insertion. The evolutionary distances among the three species have also been estimated.
This chapter discusses how the discriminant function may be applied in systematic biology. Kendall and Stuart made clear the three classes of problems involved in differentiating between two or more populations on the grounds of multivariate measurements. Discrimination concerns the problem of alloting correctly an individual to the one of k populations from which it derives. This is distinct from classification, which is concerned with classifying a sample of individuals into groups that are to be as distinct as possible, and dissection, which involves the arbitrary construction of groups. The concept of classification, as expressed in these terms, is the most commonly occurring problem in numerical taxonomy. It is only recently that professional statisticians have begun to invade this virgin ground. Gower has made a noteworthy contribution to the theory of the subject, and Jardine and Sibson have recently written a book in which the first clear formalization of some of the ideas involved is given. The chapter reviews significant biological studies in the field, some recently reanalyzed by Blackith and Reyment.
Mitochondrial DNA (mtDNA) from 131 deer mice, Peromyscus maniculatus, collected on the eight California Channel Islands and from seven southern California mainland locations, was isolated and analyzed for restriction endonuclease fragment polymorphisms. A total of 26 mtDNA genotypes were distinguishable among the deer mice sampled. All of the island samples had mtDNA restriction-fragment patterns not found among the mainland samples. Distributions of specific restriction-fragment patterns provide evidence for at least four separate colonization events to the Channel Islands. The estimated percentage of sequence divergence between all mtDNA's in this study was less than 1%, suggesting that colonization of the islands occurred fairly recently, probably within the last 500,000 years. Levels of mtDNA heterogeneity were much lower within island populations than within mainland populations.
Systematists and geneticists often wish to compare two pair-wise distance or similarity matrices based on different characters. Conventional correlation tests are not appropriate in such situations because of dependencies among the entries in each matrix. A broad class of permutation tests for association between distance matrices is described. Specific members of the class are discussed and compared using real and simulated data. Statistics resembling Kendall's tau and Spearman's rho are found to have desirable power and invariance properties.
Deer mice, Peromyscus maniculatus, collected over 90 years from three California Channel Islands, were examined for evidence of morphological change. Rapid morphological change has occurred in the endemic subspecies from Santa Barbara (P. m. elusus), Anacapa (P. m. anacapae), and Santa Cruz Island (P. m. santacruzae). Data were divided into two temporal classes, 1897-1941 and 1955-1988. Of the 16 morphological characters measured, between five and 10 measures changed significantly (P ≤ 0.05) with temporal class in each subspecies, and multivariate test statistics were significant (P ≤ 0.05) for all three subspecies. For each subspecies, depth of braincase, total length, tail length, and hind foot length became smaller over time, except depth of braincase, which became larger in P. m. elusus. The rates of change dramatically exceed those estimated from paleontological records and are even higher than those reported in some experimental selection studies. Temporal change in two characters exceeds differentiation between subspecies. Although changing, each subspecies remained well differentiated, and incorporation of temporal change allowed correct classification of most specimens. Unlike nearly all previous reports of rapid evolution, the changes in these populations were not associated with a founder events or recent introductions. This study demonstrates that rapid phenotypic change can occur in long-established natural populations and temporal stability of morphological characters in such populations, even over short evolutionary time periods, cannot be assumed.