Loss of genetic diversity and increased embryonic mortality in non‐native lizard populations

Many populations are small and isolated with limited genetic variation and high risk of mating with close relatives. Inbreeding depression is suspected to contribute to extinction of wild populations, but the historical and demographic factors that contribute to reduced population viability are often difficult to tease apart. Replicated introduction events in non‐native species can offer insights into this problem because they allow us to study how genetic variation and inbreeding depression are affected by demographic events (e.g. bottlenecks), genetic admixture and the extent and duration of isolation. Using detailed knowledge about the introduction history of 21 non‐native populations of the wall lizard Podarcis muralis in England, we show greater loss of genetic diversity (estimated from microsatellite loci) in older populations and in populations from native regions of high diversity. Loss of genetic diversity was accompanied by higher embryonic mortality in non‐native populations, suggesting that introduced populations are sufficiently inbred to jeopardize long‐term viability. However, there was no statistical correlation between population‐level genetic diversity and average embryonic mortality. Similarly, at the individual level, there was no correlation between female heterozygosity and clutch size, infertility or hatching success, or between embryo heterozygosity and mortality. We discuss these results in the context of human‐mediated introductions and how the history of introductions can play a fundamental role in influencing individual and population fitness in non‐native species.     

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.     

Founder events predict changes in genetic diversity during human‐mediated range expansions

Intentional or accidental introduction of species to new locations is predicted to result in loss of genetic variation and increase the likelihood of inbreeding, thus reducing population viability and evolutionary potential. However, multiple introductions and large founder numbers can prevent loss of genetic diversity and may therefore facilitate establishment success and range expansion. Based on a meta‐analysis of 119 introductions of 85 species of plants and animals, we here show a quantitative effect of founding history on genetic diversity in introduced populations. Both introduction of large number of individuals and multiple introduction events significantly contribute to maintaining or even increasing genetic diversity in introduced populations. The most consistent loss of genetic diversity is seen in insects and mammals, whereas introduced plant populations tend to have higher genetic variation than native populations. However, loss or gain of genetic diversity does not explain variation in the extent to which plant or animal populations become invasive outside of their native range. These results provide strong support for predictions from population genetics theory with respect to patterns of genetic diversity in introduced populations, but suggest that invasiveness is not limited by genetic bottlenecks.     

Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions

Invasive species are predicted to suffer from reductions in genetic diversity during founding events, reducing adaptive potential. Integrating evidence from two literature reviews and two case studies, we address the following questions: How much genetic diversity is lost in invasions? Do multiple introductions ameliorate this loss? Is there evidence for loss of diversity in quantitative traits? Do invaders that have experienced strong bottlenecks show adaptive evolution? How do multiple introductions influence adaptation on a landscape scale? We reviewed studies of 80 species of animals, plants, and fungi that quantified nuclear molecular diversity within introduced and source populations. Overall, there were significant losses of both allelic richness and heterozygosity in introduced populations, and large gains in diversity were rare. Evidence for multiple introductions was associated with increased diversity, and allelic variation appeared to increase over long timescales (~100 years), suggesting a role for gene flow in augmenting diversity over the long‐term. We then reviewed the literature on quantitative trait diversity and found that broad‐sense variation rarely declines in introductions, but direct comparisons of additive variance were lacking. Our studies of Hypericum canariense invasions illustrate how populations with diminished diversity may still evolve rapidly. Given the prevalence of genetic bottlenecks in successful invading populations and the potential for adaptive evolution in quantitative traits, we suggest that the disadvantages associated with founding events may have been overstated. However, our work on the successful invader Verbascum thapsus illustrates how multiple introductions may take time to commingle, instead persisting as a ‘mosaic of maladaptation’ where traits are not distributed in a pattern consistent with adaptation. We conclude that management limiting gene flow among introduced populations may reduce adaptive potential but is unlikely to prevent expansion or the evolution of novel invasive behaviour.     

Getting here from there: testing the genetic paradigm underpinning introduction histories and invasion success

Aim To explore the potential of genetic processes and mating systems to influence successful plant invasions, we compared genetic diversity of the highly invasive tropical treelet, Miconia calvescens, in nine invasive populations and three native range populations. Specifically, we tested how genetic diversity is partitioned in native and invaded regions, which have different invasion histories (multiple vs. single introductions). Lastly, we infer how levels of inbreeding in different regions impact invasion success. Location Invaded ranges in the Pacific (Hawaii, Tahiti, New Caledonia) and Australia and native range in Costa Rica. Methods Genetic diversity was inferred by analysing variation at nine microsatellite loci in 273 individuals from 13 populations of M. calvescens. Genetic structure was assessed using amova , isolation by distance (IBD) within regions, a Bayesian clustering approach, and principal coordinates analysis. Results Microsatellite analysis revealed that invaded regions exhibit low levels of allelic richness and genetic diversity with few private alleles. To the contrary, in the native range, we observed high levels of allelic richness, high heterozygosity and 78% of all private alleles. Surprisingly, despite evident genetic bottlenecks in all invasive regions, similarly high levels of inbreeding were detected in both invasive and native ranges (F_IS: 0.345 and 0.399, respectively). Bayesian clustering analysis showed a lack of geographical structure in the Pacific and evidence of differing invasion histories between the Pacific and Australia. While Pacific populations are derived from a single introduction to the region, multiple introductions have taken place in Australia from different source regions. Main conclusions Multiple introductions have not resulted in increased genetic diversity for M. calvescens invasions. Moreover, similar inbreeding levels between native and invaded ranges suggests that there is no correlation between levels of inbreeding and levels of standing genetic diversity for M. calvescens. Overall, our results show that neither inbreeding nor low genetic diversity is an impediment to invasion success.     

Low genetic diversity in the bottlenecked population of endangered non-native banteng in northern Australia

Undomesticated (wild) banteng are endangered in their native habitats in Southeast Asia. A potential conservation resource for the species is a large, wild population in Garig Gunak Barlu National Park in northern Australia, descended from 20 individuals that were released from a failed British outpost in 1849. Because of the founding bottleneck, we determined the level of genetic diversity in four subpopulations in the national park using 12 microsatellite loci, and compared this to the genetic diversity of domesticated Asian Bali cattle, wild banteng and other cattle species. We also compared the loss of genetic diversity using plausible genetic data coupled to a stochastic Leslie matrix model constructed from existing demographic data. The 53 Australian banteng sampled had average microsatellite heterozygosity (HE) of 28% compared to 67% for outbred Bos taurus and domesticated Bos javanicus populations. The Australian banteng inbreeding coefficient (F) of 0.58 is high compared to other endangered artiodactyl populations. The 95% confidence bounds for measured heterozygosity overlapped with those predicted from our stochastic Leslie matrix population model. Collectively, these results show that Australian banteng have suffered a loss of genetic diversity and are highly inbred because of the initial population bottleneck and subsequent small population sizes. We conclude that the Australian population is an important hedge against the complete loss of wild banteng, and it can augment threatened populations of banteng in their native range. This study indicates the genetic value of small populations of endangered artiodactyls established ex situ.     

Population demography and heterozygosity–fitness correlations in natural guppy populations: An examination using sexually selected fitness traits

Heterozygosity–fitness correlations (HFCs) have been examined in a wide diversity of contexts, and the results are often used to infer the role of inbreeding in natural populations. Although population demography, reflected in population‐level genetic parameters such as allelic diversity or identity disequilibrium, is expected to play a role in the emergence and detectability of HFCs, direct comparisons of variation in HFCs across many populations of the same species, with different genetic histories, are rare. Here, we examined the relationship between individual microsatellite heterozygosity and a range of sexually selected traits in 660 male guppies from 22 natural populations in Trinidad. Similar to previous studies, observed HFCs were weak overall. However, variation in HFCs among populations was high for some traits (although these variances were not statistically different from zero). Population‐level genetic parameters, specifically genetic diversity levels (number of alleles, observed/expected heterozygosity) and measures of identity disequilibrium (g2 and heterozygosity–heterozygosity correlations), were not associated with variation in population‐level HFCs. This latter result indicates that these metrics do not necessarily provide a reliable predictor of HFC effect sizes across populations. Importantly, diversity and identity disequilibrium statistics were not correlated, providing empirical evidence that these metrics capture different essential characteristics of populations. A complex genetic architecture likely underpins multiple fitness traits, including those associated with male fitness, which may have reduced our ability to detect HFCs in guppy populations. Further advances in this field would benefit from additional research to determine the demographic contexts in which HFCs are most likely to occur.     

The role of propagule pressure in the invasion success of bluegill sunfish, Lepomis macrochirus, in Japan

The bluegill sunfish, Lepomis macrochirus, is a widespread exotic species in Japan that is considered to have originated from 15 fish introduced from Guttenberg, Iowa, in 1960. Here, the genetic and phenotypic traits of Japanese populations were examined, together with 11 native populations of the USA using 10 microsatellite markers and six meristic traits. Phylogenetic analysis reconfirmed a single origin of Japanese populations, among which populations established in the 1960s were genetically close to Guttenberg population, keeping high genetic diversity comparable to the ancestral population. In contrast, genetic diversity of later-established populations significantly declined with genetic divergence from the ancestral population. Among the 1960s established populations, that from Lake Biwa showed a significant isolation-by-distance pattern with surrounding populations in which genetic bottlenecks increased with geographical distance from Lake Biwa. Although phenotypic divergence among populations was recognized in both neutral and adaptive traits, P(ST)-F(ST) comparisons showed that it is independent of neutral genetic divergence. Divergent selection was suggested in some populations from reservoirs with unstable habitats, while stabilizing selection was dominant. Accordingly, many Japanese populations of L. macrochirus appear to have derived from Lake Biwa population, expanding their distribution with population bottlenecks. Despite low propagule pressure, the invasion success of L. macrochirus is probably because of its drastic population growth in Lake Biwa shortly after its introduction, together with artificial transplantations. It not only enabled the avoidance of a loss in genetic diversity but also formed a major gene pool that supported local adaptation with high phenotypic plasticity.     

The effect of purging on sexually selected traits through antagonistic pleiotropy with survival

Sexually selected traits are expected to evolve to a point where their positive effect on reproductive success is counterbalanced by their negative effect on survival. At the genetic level, such a trade-off implies antagonistic pleiotropy between survival and the expression of sexually selected traits. Yet, the consequences of such a genetic architecture have been largely overlooked in studies examining how inbreeding influences sexually selected traits. These studies have solely interpreted their results as an effect of increased homozygosity. An alternative, however, is that purging of recessive alleles deleterious for survival when inbreeding increases can negatively affect the expression of sexually selected traits through antagonistic pleiotropy. We tested this hypothesis by analyzing the effects of inbreeding on several male ornaments and life-history traits across 20 captive populations of guppies (Poecilia reticulata) with varying levels of inbreeding. Only one ornament, orange area, decreased in its expression with an increasing level of inbreeding. This was most likely due to purging because we found no within-population relationship between orange area and the inbreeding coefficient. We further tested this hypothesis by crossing unrelated individuals from the four most inbred populations, creating a group of individuals with purged genomes but restored heterozygosity. Restoration of heterozygosity only slightly increased orange area, confirming that the decrease in orange area in the inbred populations most likely resulted from purging. These results support previous studies suggesting the existence of antagonistic pleiotropy between ornament expression and survival.     

Genome-wide genetic diversity of Holstein Friesian cattle reveals new insights into Australian and global population variability, including impact of selection

Past breeding strategies for dairy cattle have been very effective in producing rapid genetic gain to achieve industry targets and raise profitability. Such gains have been largely facilitated by intense selection of sires combined with the use of artificial insemination. However, this practice can potentially limit the level of genetic diversity through inbreeding and selection plateaus. The rate of inbreeding in Australia is increasing, primarily as a result of semen importation from a small number of prominent bulls from the USA. The effect of this genetic influx in the Australian dairy cattle population is poorly understood both in terms of diversity and local adaptation/divergence. This study uses 845 genome-wide SNP genetic markers and 431 bulls to characterize the level of genetic diversity and genetic divergence within the Australian and international Holstein Friesian dairy population. No significant differences in genetic diversity (as measured by heterozygosity [H(o)] and allelic richness [A]) were observed over the 25-year time period (1975-1999) for bulls used in Australia. The importation of foreign semen into Australia has increased the effective population size until it was in effect a sub-sample of the global population. Our data indicate that most individuals are equally closely related to one another, regardless of country of origin and year of birth. In effect, the global population can be considered as one single population unit. These results indicate that inbreeding, genetic drift and selection has had little effect at reducing genetic diversity and differentiating the Australian Holstein Friesian population at a genome-wide level.     

The change in quantitative genetic variation with inbreeding

Inbreeding is known to reduce heterozygosity of neutral genetic markers, but its impact on quantitative genetic variation is debated. Theory predicts a linear decline in additive genetic variance (V(A)) with increasing inbreeding coefficient (F) when loci underlying the trait act additively, but a nonlinear hump-shaped relationship when dominance and epistasis are important. Predictions for heritability (h2) are similar, although the exact shape depends on the value of h2 in the absence of inbreeding. We located 22 published studies in which the level of genetic variation in experimentally inbred populations (measured by V(A) or h2) was compared with that in outbred control populations. For life-history traits, the data strongly supported a nonlinear change in genetic variation with increasing F. V(A) and h2 were, respectively, 244% and 50% higher at F = 0.4 than in outbred populations, and dominance plus epistatic variance together exceeded additive variance by a factor of four. For nonfitness traits the decline was linear and estimates of nonadditive variance were small. These results confirm that population bottlenecks frequently increase V(A) in some traits, and imply that life-history traits are underlain by substantial dominance or epistasis. However, the importance of drift-induced genetic variation in conservation or evolutionary biology is questionable, in part because inbreeding depression usually accompanies inbreeding.     

Genetic diversity in natural populations of the endangered Neotropical orchid Telipogon peruvianus

Telipogon peruvianus is a highly restricted, sexually deceptive, Neotropical orchid species, endemic to the southern Peruvian Andes. It is only known from two localities, which are affected by anthropogenic disturbance. Here, we investigated whether the restricted distribution of T. peruvianus has led to low genetic diversity and inbreeding, thus threatening its survival. We isolated 10 novel microsatellite loci specific for T. peruvianus (and that also cross-amplified in related species) from two adjacent populations. We found that genetic diversity within populations was only moderately reduced, along with some evidence of inbreeding. We found low levels of genetic differentiation, suggesting connectivity by pollen/seed flow between the two populations. Effective population size was comparable to the real number of flowering individuals in the populations and we did not detect the signature of recent bottlenecks. Taken together, these results show that, despite increasing anthropogenic pressure, the two investigated populations of T. peruvianus still host valuable genetic diversity that should be preserved through appropriate conservation strategies.     

Genetic structure among morphotypes of the endangered Brazilian palm Euterpe edulis Mart (Arecaceae)

Euterpe edulis (Arecaceae) Mart has high ecological and economic importance providing food resources for more than 58 species of birds and 20 species of mammals, including humans. E. edulis is the second most exploited nontimber product from Brazilian Atlantic Forest. Due to overexploitation and destruction of habitats, E. edulis is threatened by extinction. Euterpe edulis populations have large morphological variations, with individuals having green, red, or yellow leaf sheath. However, no study has related phenotypic distinctions between populations and their levels of genetic structure. Thus, this study aimed to evaluate the diversity and genetic structure of different E. edulis morphotypes. We sampled 250 adult individuals in eight populations with the different morphotypes. Using 14 microsatellite markers, we access genetic diversity through population genetic parameters calculated in the GenAlex program and the diveRsity package in R. We used the Wilcoxon test to verify population bottlenecks and the genetic distance of Nei and Bayesian analysis for genetic clusters. The eight populations showed low allele richness, low observed heterozygosity, and high inbreeding values (f). In addition, six of the eight populations experienced genetic bottlenecks, which would partly explain the low genetic diversity in populations. Cluster analysis identified two clusters (K = 2), with green morphotype genetically distinguishing from yellow and red morphotypes. Thus, we show, for the first time, a strong genetic structure among E. edulis morphotypes even for geographically close populations.     

Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations

Understanding the genetic composition and mating systems of edge populations provides important insights into the environmental and demographic factors shaping species' distribution ranges. We analysed samples of the mangrove Avicennia marina from Vietnam, northern Philippines and Australia, with microsatellite markers. We compared genetic diversity and structure in edge (Southeast Asia, and Southern Australia) and core (North and Eastern Australia) populations, and also compared our results with previously published data from core and southern edge populations. Comparisons highlighted significantly reduced gene diversity and higher genetic structure in both margins compared to core populations, which can be attributed to very low effective population size, pollinator scarcity and high environmental pressure at distribution margins. The estimated level of inbreeding was significantly higher in northeastern populations compared to core and southern populations. This suggests that despite the high genetic load usually associated with inbreeding, inbreeding or even selfing may be advantageous in margin habitats due to the possible advantages of reproductive assurance, or local adaptation. The very high level of genetic structure and inbreeding show that populations of A. marina are functioning as independent evolutionary units more than as components of a metapopulation system connected by gene flow. The combinations of those characteristics make these peripheral populations likely to develop local adaptations and therefore to be of particular interest for conservation strategies as well as for adaptation to possible future environmental changes.     

The changes in genetic and environmental variance with inbreeding in Drosophila melanogaster

We performed a large-scale experiment on the effects of inbreeding and population bottlenecks on the additive genetic and environmental variance for morphological traits in Drosophila melanogaster. Fifty-two inbred lines were created from the progeny of single pairs, and 90 parent-offspring families on average were measured in each of these lines for six wing size and shape traits, as well as 1945 families from the outbred population from which the lines were derived. The amount of additive genetic variance has been observed to increase after such population bottlenecks in other studies; in contrast here the mean change in additive genetic variance was in very good agreement with classical additive theory, decreasing proportionally to the inbreeding coefficient of the lines. The residual, probably environmental, variance increased on average after inbreeding. Both components of variance were highly variable among inbred lines, with increases and decreases recorded for both. The variance among lines in the residual variance provides some evidence for a genetic basis of developmental stability. Changes in the phenotypic variance of these traits are largely due to changes in the genetic variance.     

Genetic variation and founder effects in the parasitoid wasp, Diaeretiella rapae (M'intosh) (Hymenoptera: Braconidae: Aphidiidae), affecting its potential as a biological control agent

The effects of recent colonization on the aphid parasitoid, Diaeretiella rapae (M'Intosh) (Hymenoptera: Braconidae: Aphidiidae), in Western Australia were investigated. When compared with populations from the Old World, the results of a microsatellite analysis show that the insects have low allelic length and low allele frequency variation, revealing that these individuals experienced a significant founder effect. Marked genetic differentiation between populations was also revealed, which has potentially important implications for host utilization in this species when introduced to a new geographical area(s). Low genetic variation and gene flow in a founder population could limit evolutionary potential in Australia, including the ability of a population to mount a response to newly introduced hosts, such as the Russian wheat aphid, Diuraphis noxia (Mordvilko). Although the actual importance of genetic diversity in the success of biological control agents is unclear, current theory concerning the potential impact of genetic bottlenecks on additive genetic variance is discussed.     

Genetic consequences of isolation: island tammar wallaby (<Emphasis Type="Italic">Macropus eugenii</Emphasis>) populations and the conservation of threatened species

Isolation and restricted gene flow can lead to genetic deterioration in populations. Populations of many species are increasingly becoming fragmented due to human impacts and active management is required to prevent further extinctions. Islands provide an ideal location to protect species from many mainland threatening processes such as habitat loss and fragmentation, disease and competition/predation from introduced species. However their isolation and small population size renders them prone to loss of genetic diversity and to inbreeding. This study examined two endemic and one introduced population of tammar wallaby (Macropus eugenii) on three islands in the Houtman Abrolhos Archipelago, Western Australia: East Wallabi (EWI), West Wallabi (WWI) and North Islands (NI). Nine autosomal and four Y-linked microsatellite loci, and sequence data from the mitochondrial DNA (mtDNA) control region were used to examine the impact of long-term isolation (EWI and WWI) and small founder size (NI) on genetic diversity and inbreeding. This study found all three populations had low genetic diversity, high levels of effective inbreeding and increased frequency of morphological abnormalities. Isolation has also led to significant inter-population genetic differentiation. These results highlight the importance of incorporating genetic management strategies when utilising islands as refuges for declining mainland populations.     

Inbreeding depression in the competitive fertilization success of male crickets

Mating between close relatives generally results in offspring of decreased fitness. Inbreeding depression is generally greater for life-history traits than for morphological traits, and recent studies of traits subject to sexual selection suggest that these may suffer the greatest inbreeding depression. Sexual selection continues after mating in the form of sperm competition and cryptic female choice, imposing strong selection on male competitive fertilization success. Here, I examine the effects of a single generation of full-sib mating on competitive fertilization success in a cricket, Teleogryllus oceanicus. The estimated coefficient of inbreeding depression in competitive fertilization success was 0.37, higher than that for other life-history and morphological traits. Such intense inbreeding depression coupled with little or no additive genetic variance for this trait is consistent with strong directional selection on male competitive fertilization success generating high levels of dominance variance, and provides an adaptive explanation for the evolution of inbreeding avoidance found in this species.     

Comparison of genetic diversity at microsatellite loci and quantitative traits in hatchery populations of Japanese flounder Paralichthys olivaceus

Relationships of genetic diversity at microsatellite loci and quantitative traits were examined in hatchery-produced populations of Japanese flounder using a relatively straightforward experiment. Five hatchery populations produced by wild-caught and domesticated broodstocks were used to examine the effects of different levels (one to three generations) of domestication on the genetic characteristics of hatchery populations. Allelic richness at seven microsatellite loci in all hatchery populations was lower than that in a wild population. Genetic variation measured by allelic richness and heterozygosity tended to decrease with an increase in generations of domestication. In addition, the degree of genetic differentiation from a wild population increased with an increase in generations of domestication. Significant differences in three morphometric traits (dorsal and anal fin ray counts and vertebral counts) and three physiological traits (high temperature, salinity and formalin tolerance) were observed among the hatchery populations. The degree of phenotypic difference among populations was larger in morphometric traits than in physiological traits. The divergence pattern of some quantitative traits was similar to that observed at microsatellite loci, suggesting that domestication causes the decrease of genetic variation and the increase of genetic differentiation for some quantitative traits concomitantly with those for microsatellite loci. Significant positive correlation was observed between F _ST and the degree of phenotypic difference in the three morphometric traits and formalin tolerance, indicating that genetic variation at microsatellite loci predicts the degree of phenotypic divergence in some quantitative traits.