Isolation and characterization of eight microsatellite loci from the house finch (Carpodacus mexicanus)

I isolated the first set of polymorphic microsatellite markers from the house finch, Carpodacus mexicanus, a well‐studied North American bird species, as part of an effort to compare levels of genetic diversity in introduced and native populations. Here, I describe eight independently assorting microsatellite loci screened for polymorphism using 40 house finches. Polymorphism levels ranged from six to 14 alleles (mean = 10.6), making these markers a powerful tool for paternity and population level analyses of this widely distributed North American species.     

Reconciling actual and inferred population histories in the house finch (Carpodacus mexicanus) by AFLP analysis

The house finch (Carpodacus mexicanus) is a native songbird of western North America that was introduced to the eastern United States and Hawaiian Islands in historic times. As such, it provides an unusually good opportunity to test the ability of molecular markers to recover recent details of a known population history. To investigate this prospect, genetic variation in 172 individuals from 16 populations in the western and eastern United States, southeastern Canada, Hawaiian Islands, and Mexico, as well as genetic variation in the closely related purple finch (Carpodacus purpureus) and Cassin's finch (Carpodacus cassinii) was studied by a semi-automated fluorescence-labeled amplified fragment length polymorphism (AFLP) marker system. A total of 363 markers were generated, of which 258 (71.2%) were polymorphic among species, 166 (61.4%) polymorphic among house finch subspecies, and 157 (60.2%) polymorphic among populations within the frontalis subspecies complex. Heterozygosities and interpopulation divergences revealed by the analysis appeared relatively low at all taxonomic levels, but there are few similar studies in avian populations with which to compare results. Whereas the known population history predicts that both eastern and Hawaiian finches should have been derived from within western populations, tree analysis using both populations and individuals as units suggests weak monophyly of eastern populations and indicates that Hawaiian populations are not clearly derived from California populations. However, the genetic distinctiveness of native and recently founded populations was disclosed by analyses of molecular variance as well as by a model-based assignment approach in which 98%, 94%, and 99% individuals from western, Hawaiian, and eastern regions, respectively, were assigned correctly to their populations without using prior information on population of origin, suggesting that these recent introductions have resulted in detectable differentiation without substantial loss of AFLP diversity. Our results indicate that AFLPs are a useful tool for population genetic and evolutionary studies of birds, particularly as a prelude to finding molecular markers linked to traits subjected to recent adaptive evolution.     

Individual variation in growth trajectories: phenotypic and genetic correlations in ontogeny of the house finch (Carpodacus mexicanus)

We studied patterns of growth in a recently established natural population of the house finch (Carpodacus mexicanus) to examine whether phenotypic and genetic covariation among age‐specific trait values is likely to constrain morphological change favoured by selection acting on adults. We found variable patterns of allometric relationships during ontogeny, and documented relatively weak covariations among ages or among traits in individual growth trajectories. Frequent compensatory growth largely cancelled out the initial differences among nestlings, potentially enabling house finches to raise offspring under diverse and unpredictable environmental conditions. Moderate levels of additive genetic variance in morphological traits throughout ontogeny, and relatively low and fluctuating phenotypic and genetic covariation among ages imply strong potential for evolutionary change in morphological traits under selection. This conclusion is consistent with the profound population‐level divergence in morphological patterns that accompanied very successful colonization of most of North America by the house finch over the last 50 years.     

Reconciling molecular signatures across markers: mitochondrial DNA confirms founder effect in invasive North American house finches (<Emphasis Type="Italic">Carpodacus mexicanus</Emphasis>)

Well-characterized species introductions provide opportunities to compare the genetic signatures of known founder effects across classes of molecular markers. The release of small numbers of house finches (Carpodacus mexicanus) into the eastern United States in the 1940s led to substantial interest in the effects of this introduction on genetic diversity in this now abundant species, an issue that has been highlighted by a recent Mycoplasma disease epidemic that most intensively affects the introduced and potentially genetically depauperate house finch populations. Previous studies comparing genetic diversity levels in native and introduced house finch populations produced seemingly disparate results: comparisons based on amplified fragment length polymorphism, RFLP mtDNA, and allozyme markers found essentially equivalent levels of diversity in eastern and western populations, whereas microsatellite markers showed clear reductions in diversity in the introduced populations. Here we employ sequence variation at the ND2 mtDNA locus to further compare levels of diversity between the four native and five introduced house finch populations that were previously examined in the microsatellite study. We found substantially lower ND2 haplotype richness and diversity across all introduced populations of house finches. The majority of sequence variation (78%) was detected within subpopulations, with the remainder (22%) explained by the historical status of each population (native or introduced). Our results are consistent with previous microsatellite evidence for a founder effect during the introduction of eastern house finches, and suggest that the mtDNA founder effect was particularly severe, likely owing to a male-biased sex ratio at the time of introduction coupled with the lower effective population size of clonally inherited markers. We discuss how the inconsistencies between past studies of house finch diversity can inform the usefulness of distinct marker sets for detecting molecular signatures of founder events.     

Microsatellite variation in simulated and natural founder populations of the Laysan finch (Telespiza cantans)

Historical and demographic data were used in a computer model tosimulate neutral genetic change in populations of the Laysanfinch (Telespiza cantans), an insular passerine bird that hasundergone documented founder events at Pearl and Hermes reef(PHR). Measures of genetic variation in the natural PHRpopulations generally matched those in the simulated populations,except that heterozygosity on Southeast Island was lower than themodel predicted, and the heterozygote excess in the naturalpopulations had a low probability of occurrence in the simulatedpopulations. The estimate of effective population size (N _e) fromthe stochastic demographic model matched the estimate fromgenetic data for two populations, but the demographic estimatewas higher than the genetic estimate for Southeast Island. Smallfounder number was rejected as a possible explanation for thereduced genetic variation on Southeast. We suggest that N _e wasoverestimated in part because we assumed seasonal variance inreproductive success. Additional variance components need to bemeasured in the field and incorporated into the model. Accounting for the heterozygote excess also requires furthertheoretical and field investigations. Possible explanations forthe excess include inbreeding depression, incest avoidance, andthe effect of polygyny on heterozygote excess in smallpopulations. We concluded that the Pearl and Hermes reefpopulation will continue to lose genetic variation at a highrate, and translocations from the native population on Laysan maybe required to maintain a viable population on the reef.     

Weak founder effect signal in a recent introduction of Caribbean Anolis

Species introductions provide a rare opportunity to study rapid evolutionary and genetic processes in natural systems, often under novel environmental pressures. Few empirical studies have been able to characterize genetic founder effects associated with demographic bottlenecks at the earliest stages of species introductions. This study utilizes prior mitochondrial DNA information which identifies the putative source population for a recently established ( c . 7 years between import and sampling) species introduction. We investigated the evidence for a founder effect in a highly successful introduction of a Puerto Rican Anolis species that has established itself on Dominica to the localized exclusion of the native, endemic anole. Five highly polymorphic microsatellite loci were used to explore the partitioning of genetic diversity within and between native source, native nonsource, and introduced populations of Anolis cristatellus . Group comparisons reveal significantly lower allelic richness and expected heterozygosity in introduced populations compared to native populations; however, tests for heterozygosity excess relative to allelic richness failed to provide consistent evidence for a founder effect within introduced populations. Significant levels of within-population genetic variation were present in both native and introduced populations. We suggest that aspects of the reproductive ecology of Anolis (high fecundity, sperm storage and multiple paternity) offer an important mechanism by which genetic variation may be maintained following demographic bottlenecks and founder events in some squamate taxa.     

Genetic variation and population structure in Scandinavian wolverine (Gulo gulo) populations

Wolverine (Gulo gulo) numbers in Scandinavia were significantly reduced during the early part of the century as a result of predator removal programmes and hunting. Protective legislation in both Sweden and Norway in the 1960s and 1970s has now resulted in increased wolverine densities in Scandinavia. We report here the development of 15 polymorphic microsatellite markers in wolverine and their use to examine the population sub-structure and genetic variability in free-ranging Scandinavian wolverine populations as well as in a sample of individuals collected before 1970. Significant subdivision between extant populations was discovered, in particular for the small and isolated population of southern Norway, which represents a recent recolonization. Overall genetic variability was found to be lower than previously reported for other mustelids, with only two to five alleles per locus and observed heterozygosities (H(O)) ranging from 0.269 to 0.376 across the examined populations, being lowest in southern Norway. Analysis of the mitochondrial DNA control region revealed no variation throughout the surveyed populations. As the historical sample did not show higher levels of genetic variability, our results are consistent with a reduction in the genetic variation in Scandinavian wolverines that pre-dates the demographic bottleneck observed during the last century. The observed subdivision between populations calls for management caution when issuing harvest quotas, especially for the geographically isolated south Norwegian population.     

Patterns of genetic diversity reveal multiple introductions and recurrent founder effects during range expansion in invasive populations of Geranium carolinianum (Geraniaceae)

Genetic diversity, and thus the adaptive potential of invasive populations, is largely based on three factors: patterns of genetic diversity in the species'' native range, the number and location of introductions and the number of founding individuals per introduction. Specifically, reductions in genetic diversity (‘founder effects'') should be stronger for species with low within-population diversity in their native range and few introductions of few individuals to the invasive range. We test these predictions with Geranium carolinianum, a winter annual herb native to North America and invasive in China. We measure the extent of founder effects using allozymes and microsatellites, and ask whether this is consistent with its colonization history and patterns of diversity in the native range. In the native range, genetic diversity is higher and structure is lower than expected based on life history traits. In China, our results provide evidence for multiple introductions near Nanjing, Jiangsu province, with subsequent range expansion to the west and south. Patterns of genetic diversity across China reveal weak founder effects that are driven largely by low-diversity populations at the expansion front, away from the introduction location. This suggests that reduced diversity in China has resulted from successive founder events during range expansion, and that the loss of genetic diversity in the Nanjing area was mitigated by multiple introductions from diverse source populations. This has implications for the future of G. carolinianum in China, as continued gene flow among populations should eventually increase genetic diversity within the more recently founded populations.     

Elevated mtDNA diversity in introduced populations of Cynotilapia afra (Günther 1894) in Lake Malawi National Park is evidence for multiple source populations and hybridization

Genetic variation in many invasive species shows little or no signs of a founder event, suggesting that high genetic diversity may facilitate establishment success. The rocky‐shore, plankton‐feeding cichlid fish Cynotilapia afra is endemic to Lake Malawi, but naturally absent from many suitable sites. In the 1960s, this species was introduced to the southern areas of the lake, presumably as a result of the aquarium fish trade. It has now become established on a number of rocky areas within the Lake Malawi National Park. Here, we analysed DNA sequence variation in the mitochondrial control region of six native and four introduced populations of C. afra, and three populations of the closely‐related and hybridizing Pseudotropheus zebra. In contrast to previous studies of Lake Malawi rock dwelling cichlids, network analyses suggested that native populations of C. afra showed high levels of lineage sorting in mtDNA. Introduced populations showed higher sequence and haplotype diversity than their native counterparts. Our analyses suggested that the elevated gene diversity was largely attributed to the fact that the introduced C. afra populations were derived from several genetically distinct and geographically separate populations, and to a lesser extent because of introgressive hybridization with native P. zebra. The establishment and spread of C. afra may be partly because of its ability to occupy a vacant ecological niche, but it may also have been facilitated by its enhanced genetic diversity.     

Microsatellite variation points to local landscape plantings as sources of invasive pampas grass (Cortaderia selloana) in California

International trade in horticultural plants is a major pathway of introduction of invasive species. Pampas grass (Cortaderia selloana) is an invasive species of horticultural origin that is native to South America but cultivated as an ornamental in regions with Mediterranean climates worldwide. To gain insight into the introduction history of invasive populations in California, we analysed microsatellite marker variation in cultivated and invasive C. selloana. We sampled 275 cultivated plants from diverse sources and 698 invasive plants from 33 populations in four geographical regions of California. A model-based Bayesian clustering analysis identified seven distinct gene pools in cultivated C. selloana. Probabilities of assignment of invasive individuals to cultivated gene pools indicated that two gene pools accounted for the genomic origin of 78% of the invasive C. selloana sampled. Extensive admixture between cultivated source gene pools was detected within invasive individuals. Sources of admixed invasive individuals are probably landscape plantings. Consistent with the Bayesian assignment results indicating that multiple cultivated gene pools and landscape plantings are probable sources of invasive populations, F(ST) and neighbour-joining clustering analyses indicated multiple escapes from shared sources in each geographical region. No isolation by distance or geographical trend in reduction of genetic diversity was evident. Furthermore, a generally random and discontinuous distribution of proportional assignments of invasive populations to cultivated gene pools suggests that introductions occurred recurrently within each geographical region. Our results strongly suggest that dispersal through local landscape plantings has contributed to the range expansion of invasive C. selloana in California.     

Molecular evidence for multiple introductions of garlic mustard (Alliaria petiolata, Brassicaceae) to North America

Invasive species offer excellent model systems for studying rapid evolutionary change. In this context, molecular markers play an important role because they provide information about pathways of introduction, the amount of genetic variation introduced, and the extent to which founder effects and inbreeding after population bottlenecks may have contributed to evolutionary change. Here, we studied microsatellite variation in eight polymorphic loci among and within 27 native and 26 introduced populations of garlic mustard (Alliaria petiolata), a European herb which is a current serious invader in North American deciduous forests. Overall, introduced populations were genetically less diverse. However, considerable variability was present and when compared to the probable source regions, no bottleneck was evident. Observed heterozygosity was very low and resulted in high inbreeding coefficients, which did not differ significantly between native and introduced populations. Thus, selfing seems to be equally dominant in both ranges. Consequently, there was strong population differentiation in the native (F(ST) = 0.704) and the introduced (F(ST) = 0.789) ranges. The high allelic diversity in the introduced range strongly suggests multiple introductions of Alliaria petiolata to North America. Out of six European regions, the British Isles, northern Europe, and central Europe had significantly higher proportions of alleles, which are common to the introduced range, and are therefore the most probable source regions. The genetic diversity established by multiple introductions, and the lack of inbreeding depression in this highly selfing species, may have contributed to the invasion success of Alliaria petiolata.     

Haplotype variation in a mitochondrial tandem repeat of Norway spruce (Picea abies) populations suggests a serious founder effect during postglacial re-colonization of the western Alps

Populations from 13 elevational transects of Norway spruce [Picea abies (L.) Karst] across the Alpine range were sampled to elucidate the geographical pattern of genetic variation in relation to postglacial re-colonization and to study elevational effects on haplotypic diversity. We assessed fragment length variation in a tandem repeat region of the mitochondrial (mt) nad1 intron 2. This maternally inherited genetic marker is suited to infer migration as it is dispersed by seed only. A total of 10 haplotypes was found, most of which were due to repeat copy number variation. An analysis of molecular variance (amova) showed that overall population differentiation was high (F(ST)=0.41), and it revealed a significant differentiation between monomorphic western and moderately to highly variable eastern Alpine populations. This phylogeographic pattern may be explained by a founder effect during postglacial re-colonization. An early arriving haplotype, assumed to originate from a western Carpathian refugium, could expand into suitable habitats, reducing the chances for establishment of subsequently arriving haplotypes. On the other hand, the high variation in populations within an Italian transect of the south-eastern Alps may be the consequence of merging migration pathways from and close distance to putative glacial refugia, most likely those assumed in the Carpathian mountains and on the Balkan peninsula or possibly in the central plains of Italy. An effect of elevation on haplotypic diversity was not evident, though a low, but significant, partition of total genetic variation was attributed to among-population variation in one Italian transect. Various factors, such as vertical seed dispersal and forest management, may account for blurring an otherwise established pattern of genetic variation on a small geographical scale.     

Molecular Evidence for Introgression and Loss of Genetic Variability in Salmo (trutta) macrostigma as a Result of Massive Restocking of Apennine Populations (Northern and Central Italy)

We assessed structural gene variation (allozymes and mtDNA) of brown trout to evaluate the genetic variability of Apennine stream populations (Northern and Central Italy) and the possibility of introgression by alien genomes after massive restocking with hatchery strains (Atlantic stocks). Genetic variability within and between Apennine populations was extremely low in our samples. Only two allozyme loci were polymorphic and mean hetero-zygosity was also reduced compared to other brown trout populations. Allelic frequencies determined for both loci were similar to the ones detected in the corresponding hatchery spawners. The reduction or total absence of the Mediterranean nuclear (LDH-5) and mitochondrial (16S rDNA) diagnostic markers suggests the domestic origin of most populations, and the introgression effects carried out by non-native genomes. From a taxonomic point of view, a clear differentiation emerges among basins placed on opposite sides of the Apennine chain (Tyrrhenian and Adriatic regions). In particular, the presence of Mediterranean genotypes and haplotypes characterizing Salmo (trutta) macrostigma is sporadic along the eastern Apennine side, adding additional doubts on the original presence and wide distribution of this salmonid along the Adriatic side of the mountain chain. In spite of conservation programs devoted to preservation of local genetic characteristics of S. t. macrostigma, massive restocking practices with hatchery strains obtained by a few spawners is the major cause of significant `founder effect' and `inbreeding depression' even in Apennine regions.     

Heterozygote excess in ancient populations of the critically endangered Dioon caputoi (Zamiaceae,Cycadales) from central Mexico

Dioon caputoi is a long‐lived cycad known from only four populations that range in size from 50 to 120, mostly adult individuals. Dioon caputoi has the most narrow geographical range of all Dioon spp. (less than 10 km), existing completely within the boundaries of the Tehuacán–Cuicatlán Biosphere Reserve, Mexico. Negative inbreeding values were found in all four populations (F_IT = ?0.242) and within subpopulations (F_IS = ?0.379). Only c. 10% of the total genetic variation was partitioned among populations (F_ST = 0.099). We also found that most mean values of genetic variation (A = 1.91 ± 0.12; P = 78.9 ± 10.2; H_E = 0.35 ± 0.01) are within the range reported for other Dioon species with larger populations and with wider geographical ranges. These results support recent findings that rare plant species maintain high levels of genetic diversity. The heterozygote excess found at all loci is discussed in detail from a neutral evolutionary perspective, leaving arguments as working hypotheses for further research. © 2008 The Linnean Society of London, Botanical Journal of the Linnean Society, 2008, 158 , 436–447.     

A contribution to characterisation of genetic variation in some natural Polish populations of Elymus repens (L.) Gould and Elymus hispidus (Opiz) Melderis (Poaceae) as revealed by RAPD markers*

To determine the relative importance of clonal growth and sexual reproduction, the Randomly Amplified Polymorphic DNA (RAPD) method was used to study genetic diversity and clonal structure of six populations of Elymus repens and four populations of Elymus hispidus from Poland. These outbreeding species are virtually self‐sterile and form widely spreading and long‐lived rhizomes. Using 12 primers, a total of 150 unambiguous RAPD fragments were amplified and scored. Results of AMOVA showed no significant genetic distinction between morphologically distinguished varieties of E. repens and E. hispidus. E. repens had slightly higher intra‐specific genetic polymorphism than E. hispidus; the percentage of polymorphic bands per population ranged from 38 to 49 and from 19 to 38 respectively. Clonal diversity measured using the Simpson diversity index (D) indicated different contributions of clonal reproduction in particular populations of E. repens (D: 0.20–0.72). Populations of E. hispidus were dominated by one or a few clones, which were generally restricted to a single population (D: 0.00–0.22). RAPD revealed that most genetic diversity resided within populations of the two studied species, suggesting that, despite their clonal character, propagation by seeds contributes considerably to reproduction of E. repens and E. hispidus.     

Absence of founder effect and evidence for adaptive divergence in a recently introduced insular population of white‐tailed deer (Odocoileus virginianus)

Islands are generally colonized by few individuals which could lead to a founder effect causing loss of genetic diversity and rapid divergence by strong genetic drift. Insular conditions can also induce new selective pressures on populations. Here, we investigated the extent of genetic differentiation within a white‐tailed deer (Odocoileus virginianus) population introduced on an island and its differentiation with its source mainland population. In response to their novel environmental conditions, introduced deer changed phenotypically from mainland individuals, therefore we investigated the genetic bases of the morphological differentiation. The study was conducted on Anticosti Island (Québec, Canada) where 220 individuals were introduced 120 years ago, resulting in a population size over 160,000 individuals. We used genotyping‐by‐sequencing (GBS) to generate 8,518 filtered high‐quality SNPs and compared patterns of genetic diversity and differentiation between the continental and Anticosti Island populations. Clustering analyses indicated a single panmictic island population and no sign of isolation by distance. Our results revealed a weak, albeit highly significant, genetic differentiation between the Anticosti Island population and its source population (mean F_ST = 0.005), which allowed a population assignment success of 93%. Also, the high genetic diversity maintained in the introduced population supports the absence of a strong founder effect due to the large number of founders followed by rapid population growth. We further used a polygenic approach to assess the genetic bases of the divergent phenotypical traits between insular and continental populations. We found loci related to muscular function and lipid metabolism, which suggested that these could be involved in local adaptation on Anticosti Island. We discuss these results in a harvest management context.     

Genetic and morphometric evidence on a Galápagos Island exposes founder effects and diversification in the first‐known (truly) feral western dog population

Domesticated animals that revert to a wild state can become invasive and significantly impact native biodiversity. Although dogs can be problematic locally, only the Australasian dingo is known to occur in isolation from humans. Western dogs have experienced more intense artificial selection, which potentially limits their invasiveness. However, feral dogs eradicated from Isabela Island, Galápagos in the 1980s could be the first‐known exception. We used DNA and morphometric data from 92 of these dogs to test the hypotheses that (i) these dogs persisted independently of humans for up to a century and a half since descending from a handful of dogs introduced in the early 1800s, vs. (ii) similarly to other western feral dog populations, they reflected continuous recruitment of strays from human settlements on a portion of the Island. We detected one dominant maternal lineage and one dominant paternal lineage shared by the three subpopulations, along with low autosomal genetic diversity, consistent with the hypothesized common origins from a small founder population. Genetic diversity patterns among the three island subpopulations were consistent with stepping‐stone founder effects, while morphometric differentiation suggested rapid phenotypic divergence, possibly due to drift and reinforced by selection corresponding to distinct microclimates and habitats on Isabela. Despite the continued presence of free‐ranging dogs in the vicinity of settlements on Isabela and other Galápagos Islands, feral populations have not reestablished in remote areas since the 1980s, emphasizing the rarity of conditions necessary for feralization of modern western dogs.     

Small founding number and low genetic diversity in an introduced species exhibiting limited invasion success (speckled dace, Rhinichthys osculus)

Molecular evaluations of successful invaders are common, however studies of introduced species that have had limited invasion success, or have died out completely, are rare. We studied an introduced population of speckled dace (Rhinichthys osculus) from northern California, USA that has rapidly increased in abundance but remained restricted to a 25-km stretch of river since its introduction in the mid-1980s. Field and laboratory analyses indicate that invasion success of speckled dace is constrained by the combined effects of multiple predators. The role of bottleneck effects associated with the introduction has not been studied. We assayed variation in seven microsatellite loci and one mitochondrial DNA gene in the introduced population and nine putative source populations to identify the source population and evaluate bottleneck effects. The Trinity River system was supported as the source owing to its genetic similarity and geographic proximity to the introduced population. Consistent with a bottleneck, the introduced population exhibited reduced allelic and haplotype richness in comparison to source populations. Estimates of the genetically effective number of individuals founding the introduced population using nuclear coalescent analyses and a mitochondrial simulation procedure were highly concordant in suggesting that the initial colonizing group was comprised of about 10 individuals. A bottleneck effect in an exotic species exhibiting limited invasion success has rarely been documented and thus introduction of speckled dace represents an important model system for future investigation. Establishing a relationship between genetic diversity and factors limiting invasion success in this system (e.g., predator avoidance) will help determine the extent to which genetic diversity loss has constrained invasion success in speckled dace.