Role of propagule pressure in colonization success: disentangling the relative importance of demographic,genetic and habitat effects

High propagule pressure is arguably the only consistent predictor of colonization success. More individuals enhance colonization success because they aid in overcoming demographic consequences of small population size (e.g. stochasticity and Allee effects). The number of founders can also have direct genetic effects: with fewer individuals, more inbreeding and thus inbreeding depression will occur, whereas more individuals typically harbour greater genetic variation. Thus, the demographic and genetic components of propagule pressure are interrelated, making it difficult to understand which mechanisms are most important in determining colonization success. We experimentally disentangled the demographic and genetic components of propagule pressure by manipulating the number of founders (fewer or more), and genetic background (inbred or outbred) of individuals released in a series of three complementary experiments. We used Bemisia whiteflies and released them onto either their natal host (benign) or a novel host (challenging). Our experiments revealed that having more founding individuals and those individuals being outbred both increased the number of adults produced, but that only genetic background consistently shaped net reproductive rate of experimental populations. Environment was also important and interacted with propagule size to determine the number of adults produced. Quality of the environment interacted also with genetic background to determine establishment success, with a more pronounced effect of inbreeding depression in harsh environments. This interaction did not hold for the net reproductive rate. These data show that the positive effect of propagule pressure on founding success can be driven as much by underlying genetic processes as by demographics. Genetic effects can be immediate and have sizable effects on fitness.     

Hidden founder effects: small‐scale spatial genetic structure in recently established populations of the grassland specialist plant Anthyllis vulneraria

The long‐term establishment success of founder plant populations has been commonly assessed based on the measures of population genetic diversity and among population genetic differentiation, with founder populations expected to carry sufficient genetic diversity when population establishment is the result of many colonists from multiple source populations (the ‘migrant pool’ colonization model). Theory, however, predicts that, after initial colonization, rapid population expansion may result in a fast increase in the extent of spatial genetic structure (SGS), independent of extant genetic diversity. This SGS can reduce long‐term population viability by increasing inbreeding. Using 12 microsatellite markers, we inferred colonization patterns in four recent populations of the grassland specialist plant Anthyllis vulneraria and compared the extent of SGS between recently established and old populations. Assignment analyses of the individuals of recent population based on the genetic composition of nine adjacent putative source populations suggested the occurrence of the ‘migrant pool’ colonization model, further confirmed by high genetic diversity within and low genetic differentiation among recent populations. Population establishment, however, resulted in the build‐up of strong SGS, most likely as a result of spatially restricted recruitment of the progeny of initial colonists. Although reduced, significant SGS was nonetheless observed to persist in old populations. The presence of SGS was in all populations associated with elevated inbreeding coefficients, potentially affecting the long‐term viability of these populations. In conclusion, this study illustrates the importance of studying SGS next to population genetic diversity and differentiation to adequately infer colonization patterns and long‐term establishment success of plant species.     

Genetic and demographic founder effects have long‐term fitness consequences for colonising populations

Colonisation is a fundamental ecological and evolutionary process that drives the distribution and abundance of organisms. The initial ability of colonists to establish is determined largely by the number of founders and their genetic background. We explore the importance of these demographic and genetic properties for longer term persistence and adaptation of populations colonising a novel habitat using experimental populations of Tribolium castaneum. We introduced individuals from three genetic backgrounds (inbred – outbred) into a novel environment at three founding sizes (2–32), and tracked populations for seven generations. Inbreeding had negative effects, whereas outbreeding generally had positive effects on establishment, population growth and long‐term persistence. Severe bottlenecks due to small founding sizes reduced genetic variation and fitness but did not prevent adaptation if the founders originated from genetically diverse populations. Thus, we find important and largely independent roles for both demographic and genetic processes in driving colonisation success.     

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.     

Genetic diversity of a successful colonizer: isolated populations of Metrioptera roeselii regain variation at an unusually rapid rate

Newly founded isolated populations need to overcome detrimental effects of low genetic diversity. The establishment success of a population may therefore depend on various mechanisms such as assortative mating, purging of deleterious alleles, creation of new mutations and/or repeated inflow of new genotypes to reduce the effects of inbreeding and further loss of genetic variation. We compared the level of genetic variation in introduced populations of an insect species (Metrioptera roeselii) far beyond its natural distribution with levels found in their respective founder populations and coupled the data with timing since establishment. This allowed us to analyze if the introduced populations showed signs of temporal changes in genetic variation and have made it possible to evaluate underlying mechanisms. For this, we used neutral genetic markers, seven microsatellite loci and a 676–bp‐long sequence of the mtDNA COI gene. All tested indices (allelic richness, unbiased expected heterozygosity, effective size, haplotype diversity, and nucleotide diversity) except inbreeding coefficient had significantly higher values in populations within the founding populations inside the continuous area of the species distribution compared with the introduced populations. A logarithmic model showed a significant correlation of both allelic richness and unbiased expected heterozygosity with age of the isolated populations. Considering the species' inferred colonization history and likely introduction pathways, we suggest that multiple introductions are the main mechanism behind the temporal pattern observed. However, we argue that influences of assortative mating, directional selection, and effects of an exceptional high intrapopulation mutation rate may have impacts. The ability to regain genetic diversity at this level may be one of the main reasons why M. roeselii successfully continue to colonize northern Europe.     

Early colonisation population structure of a Norway rat island invasion

Colonists undergo non-equilibrium processes such as founder effects, inbreeding and changing population size which influence the mating system and demography of a population. Understanding these processes in colonising populations informs management and helps prevent further invasions. We sampled and genotyped most individuals of a Norway rat (Rattus norvegicus) reinvasion on Moturemu island (5 ha) in New Zealand. Population size was most likely between 30 and 33 rats. Genetic methods detected a clear bottleneck signal from the founding population. Parentage assignment revealed promiscuous mating dominated by a few individuals with increasing inbreeding, both putatively a result of small island size. Combining ecological and genetic data from a single sample allowed inferences on population structure and functioning. Invading Norway rats rapidly achieve population structure similar to established island populations despite a small number of colonists and associated inbreeding. Overcoming these initial obstacles to population establishment contributes to the global success of invasive rats.     

Genetic rescue and inbreeding depression in Mexican wolves

Although inbreeding can reduce individual fitness and contribute to population extinction, gene flow between inbred but unrelated populations may overcome these effects. Among extant Mexican wolves (Canis lupus baileyi), inbreeding had reduced genetic diversity and potentially lowered fitness, and as a result, three unrelated captive wolf lineages were merged beginning in 1995. We examined the effect of inbreeding and the merging of the founding lineages on three fitness traits in the captive population and on litter size in the reintroduced population. We found little evidence of inbreeding depression among captive wolves of the founding lineages, but large fitness increases, genetic rescue, for all traits examined among F1 offspring of the founding lineages. In addition, we observed strong inbreeding depression among wolves descended from F1 wolves. These results suggest a high load of deleterious alleles in the McBride lineage, the largest of the founding lineages. In the wild, reintroduced population, there were large fitness differences between McBride wolves and wolves with ancestry from two or more lineages, again indicating a genetic rescue. The low litter and pack sizes observed in the wild population are consistent with this genetic load, but it appears that there is still potential to establish vigorous wild populations.     

Prior adaptation,diversity, and introduction frequency mediate the positive relationship between propagule pressure and the initial success of founding populations

Propagule pressure is often considered the most consistent predictor of the success of founding populations. This relationship could be mediated by the composition of the founding group (e.g. level of prior adaptation to the recipient environment or its diversity) as well as the introduction scenario (i.e. the frequency, size and timing of discrete introduction events). We introduced groups of Tribolium castaneum (red flour beetle) eggs across three levels of propagule pressure (n?=?15, 30, 60), of three possible compositions (single, adapted lineage; single, unadapted lineage; mixed lineages) to a novel environment using six unique introduction scenarios, in a fully factorial design to evaluate the importance of composition and introduction scenario in influencing the relationship between propagule pressure and establishment. In our system, prior adaptation to the environment, including having some adapted individuals in mixed groups, rivaled the importance of propagule pressure in determining the establishment success and size of founding populations. More frequent introduction events resulted in fewer individuals that initially survived founding, but introduction scenario did not significantly influence establishment success or population size. This experimental evidence demonstrates the importance of context, both of the founding group and the recipient environment, in understanding how propagule pressure influences the success of founding populations.     

Shifting dispersal modes at an expanding species’ range margin

While it is generally recognized that noncontiguous (long‐distance) dispersal of small numbers of individuals is important for range expansion over large geographic areas, it is often assumed that colonization on more local scales proceeds by population expansion and diffusion dispersal (larger numbers of individuals colonizing adjacent sites). There are few empirical studies of dispersal modes at the front of expanding ranges, and very little information is available on dispersal dynamics at smaller geographic scales where we expect contiguous (diffusion) dispersal to be prevalent. We used highly polymorphic genetic markers to characterize dispersal modes at a local geographic scale for populations at the edge of the range of a newly invasive grass species (Brachypodium sylvaticum) that is undergoing rapid range expansion in the Pacific Northwest of North America. Comparisons of Bayesian clustering of populations, patterns of genetic diversity, and gametic disequilibrium indicate that new populations are colonized ahead of the invasion front by noncontiguous dispersal from source populations, with admixture occurring as populations age. This pattern of noncontiguous colonization was maintained even at a local scale. Absence of evidence for dispersal among adjacent pioneer sites at the edge of the expanding range of this species suggests that pioneer populations undergo an establishment phase during which they do not contribute emigrants for colonization of neighbouring sites. Our data indicate that dispersal modes change as the invasion matures: initial colonization processes appear to be dominated by noncontiguous dispersal from only a few sources, while contiguous dispersal may play a greater role once populations become established.     

Recovery process of genetic diversity through seed and pollen immigration at the northernmost leading-edge population of Fagus crenata

The range expansion of a plant species begins with colonization of ecological empty patches from posterior source populations. This process involves stochastic loss of genetic diversity. However, the founder population could restore genetic diversity by gene flow from posterior populations via seeds and pollen and its recovery affects evolutionary potential for species expansion. To clarify the recovery process of genetic diversity during species range expansion, gene flow via seeds and pollen was investigated at the expansion front of Fagus crenata. Based on eight nuclear microsatellite genotypes of a total of 150 individuals and 225 seeds at the northernmost leading-edge population, genetic diversity, fine-scale spatial genetic structure (FSGS), and genetic differentiation from other five northern populations were investigated. Moreover, both seed and pollen immigration and their effects on genetic diversity at different successional stages were analyzed. The leading-edge population showed lower genetic diversity and substantial genetic differentiation, reflecting its strong genetic drift. Non-significant FSGS and a negative inbreeding coefficient for mature trees may indicate that the earliest generation consisted of founders from foreign seed sources. The significant proportion of seed and pollen immigration increased the number of different alleles for later successional stages. The effective number of pollen parents from foreign sources (20.8) was markedly higher than that from the local source (2.1). These results indicated that pollen immigration incorporated new and rare alleles and increased the genetic diversity of the population. However, the proportion of foreign gene flow decreased during succession, probably due to the increased reproductive success of local individuals as they reached maturity and grew in size.     

Population‐level traits that affect,and do not affect,invasion success

What allows some species to successfully colonize a novel environment while others fail? Numerous studies in invasion biology have sought to answer this question, but those studies have tended to focus on traits of species or individuals (e.g. body size, seed size, seed number), and these traits have largely been found to be weak predictors of invasion success. However, characteristics of colonizing populations (e.g. genetic diversity, density, age structure) might also be important for successful establishment, as the authors of a study published in this issue of Molecular Ecology show ( Crawford & Whitney 2010 ). By experimentally manipulating the density and genetic diversity of colonizing populations of Arabidopsis thaliana, the authors found that genetic diversity, but not population density, increased colonization success. Importantly, the effects of genetic diversity on colonization success were both additive and non‐additive, suggesting that traits associated with particular genotypes and complimentarity among genotypes contribute to colonization success. This research highlights the importance of considering within‐species variation and characteristics of entire populations in predicting colonization success.     

Patterns of genetic diversity in colonizing plant species: Nassauvia lagascae var. lanata (Asteraceae: Mutisieae) on Volcan Lonquimay, Chile

The effect of colonization on the distribution of genetic diversity within and among populations in relation to species characteristics remains an open empirical question. The objective of this study was to contrast genetic diversity within and among established and colonizing populations of Nassauvia lagascae var. lanata on Volcán Lonquimay (Araucanía Region, Chile), which erupted on 25 December 1988, and relate genetic diversity to biological characteristics of the populations. We analyzed a total of 240 individuals from 15 populations distributed along the Andes Cordillera using AFLP and obtained a total of 307 AFLP bands, of which 97.7% are polymorphic. Values of population differentiation (F(ST)) did not differ significantly among established and colonizing populations, but colonizing populations did have reduced levels of genetic divergence (as indicated by private and rare bands) and genetic variation (e.g., Shannon index). We conclude that a founder effect through limited numbers of founding propagules derived from nearby source populations has not yet been compensated for by subsequent population growth and migration. Low rates of secondary dispersal via running water, kin-structure within populations, and slow population growth seem to contribute to the slow recovery of genetic diversity.     

Colonization in action: genetic characteristics of <Emphasis Type="Italic">Daphnia magna</Emphasis> Strauss (Crustacea,Anomopoda) in two recently restored ponds

New habitats are an interesting tool to monitor colonization processes in the light of changes in genetic structure and evolutionary potential of populations. Cladocerans are cyclical parthenogens that offer the possibility to track genetic changes during the colonization process due to the alternation of sexual and asexual phases. The locally called “malladas” are shallow and temporary peridunal ponds in Eastern Spain that were silted in the 1960s and have been recently dug to their original basin. We here describe the colonization process in two of these newly restored ponds by the cladoceran Daphnia magna during their first 3 years. This colonization process followed three critical steps: population founding by the initial colonists, arrival of secondary immigrants and consolidation of the population structure. We found a low number of genotype colonists followed by the establishment of secondary immigrants and a slight decrease in gene flow with time. We discuss the importance of dispersal, founder effects, natural selection, inbreeding depression and genetic drift during the colonization process in the light of the most recent literature.     

Genetic rescue in a severely inbred wolf population

Natural populations are becoming increasingly fragmented which is expected to affect their viability due to inbreeding depression, reduced genetic diversity and increased sensitivity to demographic and environmental stochasticity. In small and highly inbred populations, the introduction of only a few immigrants may increase vital rates significantly. However, very few studies have quantified the long‐term success of immigrants and inbred individuals in natural populations. Following an episode of natural immigration to the isolated, severely inbred Scandinavian wolf (Canis lupus) population, we demonstrate significantly higher pairing and breeding success for offspring to immigrants compared to offspring from native, inbred pairs. We argue that inbreeding depression is the underlying mechanism for the profound difference in breeding success. Highly inbred wolves may have lower survival during natal dispersal as well as competitive disadvantage to find a partner. Our study is one of the first to quantify and compare the reproductive success of first‐generation offspring from migrants vs. native, inbred individuals in a natural population. Indeed, our data demonstrate the profound impact single immigrants can have in small, inbred populations, and represent one of very few documented cases of genetic rescue in a population of large carnivores.     

Benefits of increased colonist quantity and genetic diversity for colonization depend on colonist identity

Larger numbers of colonists can be more likely to establish and spread due to the benefits provided by either more individuals (quantity) or a greater diversity of genotypes or phenotypes (genetic diversity). However, the value of higher colonist quantity or genetic diversity varies widely across studies, leaving a great deal of uncertainty in how these respective mechanisms affect colonization success. This variability is potentially driven by differences in which traits are present in respective colonist pools (‘colonist identity’). Studies with high‐performing colonizers (e.g. genotypes pre‐adapted to the colonizing environment) may find increasing quantity or diversity to be beneficial because it increases the chance high‐performers are sampled, while studies with no high‐performers may find no effects of quantity or diversity. Alternatively, quantity and genetic diversity may play little to no role if the smallest populations already contain high‐performing colonists because there is no scope for a sampling effect to operate. We conducted a field mesocosm experiment to determine if variability in the benefits provided by increased quantity or genetic diversity relates to colonist traits. Nine distinct genotypes of Daphnia pulex characterized also by phenotype, were introduced in ‘single’ (one individual) or ‘many’ (nine individuals) introduction quantities and at ‘low’ (monoclonal) and ‘high’ (mixed genotypes) genetic diversities. We found that larger‐bodied D. pulex genotypes benefited less from increased colonist quantity, while increasing genetic diversity tended to have a lower effect on higher growth rate genotypes. Our results show that the trait values of the colonists can determine the benefits gained when colonist quantity or genetic diversity are increased, with potential applications to future research and practical efforts to promote, or prevent, population establishment.     

Role of evolutionary and ecological factors in the reproductive success and the spatial genetic structure of the temperate gorgonian Paramuricea clavata

Dispersal and mating features strongly influence the evolutionary dynamics and the spatial genetic structure (SGS) of marine populations. For the first time in a marine invertebrate, we examined individual reproductive success, by conducting larval paternity assignments after a natural spawning event, combined with a small‐scale SGS analysis within a population of the gorgonian Paramuricea clavata. Thirty four percent of the larvae were sired by male colonies surrounding the brooding female colonies, revealing that the bulk of the mating was accomplished by males from outside the studied area. Male success increased with male height and decreased with increasing male to female distance. The parentage analyses, with a strong level of self‐recruitment (25%), unveiled the occurrence of a complex family structure at a small spatial scale, consistent with the limited larval dispersal of this species. However, no evidence of small scale SGS was revealed despite this family structure. Furthermore, temporal genetic structure was not observed, which appears to be related to the rather large effective population size. The low level of inbreeding found suggests a pattern of random mating in this species, which disagrees with expectations that limited larval dispersal should lead to biparental inbreeding. Surface brooding and investment in sexual reproduction in P. clavata contribute to multiple paternity (on average 6.4 fathers were assigned per brood), which enhance genetic diversity of the brood. Several factors may have contributed to the lack of biparental inbreeding in our study such as (i) the lack of sperm limitation at a small scale, (ii) multiple paternity, and (iii) the large effective population size. Thus, our results indicate that limited larval dispersal and complex family structure do not necessarily lead to biparental inbreeding and SGS. In the framework of conservation purposes, our results suggested that colony size, proximity among colonies and the population size should be taken into consideration for restoration projects.     

Effects of inbreeding on life history and thermal performance in the tropical butterfly Bicyclus anynana

Human-induced loss and fragmentation of natural habitats reduces population size and thereby presumably genetic diversity through inbreeding or genetic drift. Additionally, many species are confronted with increased temperature stress due to climate change, with reduced genetic diversity potentially interfering with a species’ ability to cope with such conditions. While in general the detrimental impact of inbreeding has often been documented, its consequences for the ability to cope with temperature stress are still poorly understood. Against this background we here investigate the effects of inbreeding on egg hatching success, development and temperature stress tolerance in the tropical butterfly Bicyclus anynana. Specifically we test for an increased sensitivity to environmental stress in inbred individuals. Our results revealed that even comparatively low levels of inbreeding yield negative consequences for reproduction and development under beneficial conditions. Inbreeding also reduced cold tolerance in adult butterflies, while heat tolerance remained unaffected. We therefore conclude that acute stress tolerance may not be generally impaired by inbreeding.     

Past bottlenecks and current population fragmentation of endangered huemul deer (<Emphasis Type="Italic">Hippocamelus bisulcus</Emphasis>): implications for preservation of genetic diversity

Small populations in fragmented habitats can lose genetic variation through drift and inbreeding. The huemul (Hippocamelus bisulcus) is an endangered deer endemic to the southern Andes of Chile and Argentina. Huemul numbers have declined by 99% and its distribution by 50% since European settlement. The total population is estimated at less than 2,000 individuals and is highly fragmented. At one isolated population in Chilean Patagonia we sampled 56 individuals between 2005 and 2007 and genotyped them at 14 microsatellite loci. Despite low genetic variability (average 2.071 alleles/locus and average H _O of 0.341), a low inbreeding coefficient (F _IS) of 0.009 suggests nearly random mating. Population genetic bottleneck tests suggest both historical and contemporary reductions in population size. Simulations indicated that the population must be maintained at 75% of the current size of 120 individuals to maintain 90% of its current genetic diversity over the next 100 years. Potential management strategies to maintain genetic variability and limit future inbreeding include the conservation and establishment of habitat corridors to facilitate gene flow and the enlargement of protected areas to increase effective population size.     

Cryptic inbreeding depression in a growing population of a long‐lived species

Genetic effects are often overlooked in endangered species monitoring, and populations showing positive growth are often assumed to be secure. However, the continued reproductive success of a few individuals may mask issues such as inbreeding depression, especially in long‐lived species. Here, we test for inbreeding depression in little spotted kiwi (Apteryx owenii) by comparing a population founded with two birds to one founded with 40 birds, both from the same source population and both showing positive population growth. We used a combination of microsatellite genotypes, nest observations and modelling to examine the consequences of assessing population viability exclusively via population growth. We demonstrate (i) significantly lower hatching success despite significantly higher reproductive effort in the population with two founders; (ii) positive growth in the population with two founders is mainly driven by ongoing chick production of the founding pair; and (iii) a substantial genetic load in the population founded with two birds (10–15 diploid lethal equivalents). Our results illustrate that substantial, cryptic inbreeding depression may still be present when a population is growing, especially in long‐lived species with overlapping generations.     

Genome‐scale data reveal that endemic Poecilia populations from small sulphidic springs display no evidence of inbreeding

Populations with limited ranges can be highly vulnerable to changes in their environment and are, thus, of high conservation concern. Populations that experience human‐induced range reductions are often highly inbred and lack genetic diversity, but it is unknown whether this is also the case for populations with naturally small ranges. The fishes Poecilia sulphuraria (listed as critically endangered) and Poecilia thermalis, which are endemic to small hydrogen sulphide‐rich springs in southern Mexico, are examples of such populations with inherently small habitats. We used geometric morphometrics and population genetics to quantify phenotypic and genetic variation within and among two populations of P. sulphuraria and one population of P. thermalis. Principal component analyses revealed phenotypic and genetic differences among the populations. Evidence for inbreeding was low compared to populations that have undergone habitat reduction. The genetic data were also used to infer the demographic history of these populations to obtain estimates for effective population sizes and migration rates. Effective population sizes were large given the small habitats of these populations. Our results imply that these three endemic extremophile populations should each be considered separately for conservation purposes. Additionally, this study suggests that populations in naturally small habitats may have lower rates of inbreeding and higher genetic diversity than expected, and therefore may be better equipped to handle environmental perturbations than anticipated. We caution, however, that the inferred lack of inbreeding and the large effective population sizes could potentially be a result of colonization by genetically diverse ancestors.