How do reproductive skew and founder group size affect genetic diversity in reintroduced populations?

Reduced genetic diversity can result in short-term decreases in fitness and reduced adaptive potential, which may lead to an increased extinction risk. Therefore, maintaining genetic variation is important for the short- and long-term success of reintroduced populations. Here, we evaluate how founder group size and variance in male reproductive success influence the long-term maintenance of genetic diversity after reintroduction. We used microsatellite data to quantify the loss of heterozygosity and allelic diversity in the founder groups from three reintroductions of tuatara ( Sphenodon ), the sole living representatives of the reptilian order Rhynchocephalia. We then estimated the maintenance of genetic diversity over 400 years (∼10 generations) using population viability analyses. Reproduction of tuatara is highly skewed, with as few as 30% of males mating across years. Predicted losses of heterozygosity over 10 generations were low (1–14%), and populations founded with more animals retained a greater proportion of the heterozygosity and allelic diversity of their source populations and founder groups. Greater male reproductive skew led to greater predicted losses of genetic diversity over 10 generations, but only accelerated the loss of genetic diversity at small population size (<250 animals). A reduction in reproductive skew at low density may facilitate the maintenance of genetic diversity in small reintroduced populations. If reproductive skew is high and density-independent, larger founder groups could be released to achieve genetic goals for management.     

Ancient,but not recent,population declines have had a genetic impact on alpine yellow-bellied toad populations,suggesting potential for complete recovery

Reduction in population size and local extinctions have been reported for the yellow-bellied toad, Bombina variegata, but the genetic impact of this is not yet known. In this study, we genotyped 200 individuals, using mtDNA cytochrome b and 11 nuclear microsatellites. We investigated fine-scale population structure and tested for genetic signatures of historical and recent population decline, using several statistical approaches, including likelihood methods and approximate Bayesian computation. Five major genetically divergent groups were found, largely corresponding to geography but with a clear exception of high genetic isolation in a highly touristic area. The effective sizes in the last few generations, as estimated from the random association among markers, never exceeded a few dozen of individuals. Our most important result is that several analyses converge in suggesting that genetic variation was shaped in all groups by a 7- to 45-fold demographic decline, which occurred between a few hundred and a few 1000 years ago. Remarkably, only weak evidence supports recent genetic impact related to human activities. We believe that the alpine B. variegata populations should be monitored and protected to stop their recent decline and to prevent local extinctions, with highest priority given to genetically isolated populations. Nonetheless, current genetic variation pattern, being mostly shaped in earlier times, suggests that complete recovery can be achieved. In general, our study is an example of how the potential for recovery should be inferred even under the co-occurrence of population decline, low genetic variation, and genetic bottleneck signals.     

Endemism and ecological islands: the ostracods from Jamaican bromeliads

1. The inhabitants of ecological islands, such as the phytolemata of bromeliad plants, provide an opportunity to examine the genetic patterns resulting from island radiations and draw inferences about modes of speciation.
2. Allozyme electrophoresis, as well as mitochondrial DNA and morphological analyses, were employed to delimit species boundaries and assess the population genetic structure of the ostracods from bromeliads on the island of Jamaica.
3. Nine species from the genus Elpidium were both sexually reproducing and endemic to the island. The other commonly encountered ostracod genus, Candonopsis , was represented by at least two sexually reproducing species.
4. Most Elpidium species showed very restricted distributions, low heterozygosity, and marked gene pool fragmentation, suggesting that population bottlenecks have occurred frequently. Whether founder events played a causal role in the diversification of these ostracods remains uncertain, but bromeliad habitats seem to be a source of high biodiversity, and may represent an ideal setting for extensive allopatric speciation.     

Endemism and ecological islands: the ostracods from Jamaican bromeliads

1. The inhabitants of ecological islands, such as the phytolemata of bromeliad plants, provide an opportunity to examine the genetic patterns resulting from island radiations and draw inferences about modes of speciation.
2. Allozyme electrophoresis, as well as mitochondrial DNA and morphological analyses, were employed to delimit species boundaries and assess the population genetic structure of the ostracods from bromeliads on the island of Jamaica.
3. Nine species from the genus Elpidium were both sexually reproducing and endemic to the island. The other commonly encountered ostracod genus, Candonopsis , was represented by at least two sexually reproducing species.
4. Most Elpidium species showed very restricted distributions, low heterozygosity, and marked gene pool fragmentation, suggesting that population bottlenecks have occurred frequently. Whether founder events played a causal role in the diversification of these ostracods remains uncertain, but bromeliad habitats seem to be a source of high biodiversity, and may represent an ideal setting for extensive allopatric speciation.     

Genetic management of the red squirrel,Sciurus vulgaris: a practical approach to regional conservation

The progressive decline in red squirrel (Sciurus vulgaris) numbers in Wales has led to conservation and reintroduction projects being established on the island of Anglesey. The recovery of the island’s remnant wild population was initially successful, however concern remained over potential loss of genetic diversity resulting from an observed demographic bottleneck. We used mitochondrial DNA (mtDNA) control region sequences and six microsatellite loci to assess current levels of genetic variation in the population. Samples were monomorphic for control region sequences and a historic specimen from the same area carrying a different haplotype demonstrated a loss of mtDNA diversity during the last 20 years. Inclusion of other Welsh haplotypes indicated phylogeographic structure in the region, in contrast to previous UK studies. Genotyping results showed allelic diversity and heterozygosity to be less than 50% of that recorded in other UK populations, with strong evidence for a recent genetic bottleneck. A parallel reintroduction programme on Anglesey included genetic analysis of individuals during the selection of captive breeding pairs. We present analysis of sequence and microsatellite data, and subsequent management decisions taken to maximise diversity in the founder and F1 generations. Population and Habitat Viability Analysis applied to both populations modelled future levels of heterozygosity and allelic diversity. Supplementation of the remnant and reintroduced populations with translocated squirrels was simulated as a potential management tool; results support use of this strategy to reduce loss of diversity and increase survival. The limitations of applying conservation genetic theory within small-scale management projects are discussed.     

Identity by Descent in Island-Mainland Populations

A new model is presented for the genetic structure among a collection of island populations, with fluctuating population sizes and continuous overlapping generations, using a stochastic birth, death and immigration (BDI) process. Immigrants enter each island from a large mainland population, with constant gene frequencies, according to a Poisson process. The average probability of identity by descent (IBD) for two haploid individuals randomly selected from an island population is f(0) = (f(1) + λ)/( + λ), where f(1) is the probability of IBD for two randomly selected immigrants, λ is the birth-rate for each individual, and is the arrival rate of immigrants into each island. The value of f(0) is independent of the death process, time and N. The expected level of genetic differentiation among island populations is F(ST) = (1 - 1/n)λ/( + λ), where n is the total number of islands receiving immigrants. Because f(0) and F(ST) are independent of the death process, for a BDI model, the population genetic structure for several general demographic situations may be examined using our equations. These include stochastic exponential, or logistic (regulated by death rate) growth within islands, or a ``source-sink' population structure. Because the expected values of both f(0) and F(ST) are independent of time, these are achieved immediately, for a BDI model, with no need to assume the island populations are at genetic equilibrium.     

Modeling the adaptive potential of isolated populations: experimental simulations using Drosophila

The genetic variability underlying many morphological and stress resistance traits may largely depend on the effects of genetic drift balanced by polygenic mutation. This model of adaptive potential has played a central role in the minimum viable population size concept and has been used to predict the effective population size necessary to prevent extinction within changing environments. However, there have been few long-term experimental studies of adaptive potential within isolated populations, and no study has thus far provided an experimental test of the drift-mutation model of quantitative genetic variation. Using the sternopleural bristle number of Drosophila melanogaster as a model quantitative trait, we performed repeated measurements of adaptive potential on 15 replicate populations of two and 10 male-female pairs over 30 and 77 generations, respectively. Declines in adaptive potential were analyzed by comparing observed and expected changes in realized heritability over time. The only significant model deviation occurred immediately after bottlenecks of two pairs, in which greater than expected declines in realized heritability were observed. This result suggests that changes in allelic diversity during bottleneck events may be as important as changes in heterozygosity in determining adaptive potential. Drift-mutation model expectations were otherwise realized over all generations. Our results validate the use of the drift-mutation model as a tool for understanding the dynamics of adaptive potential for peripheral fitness characters, but suggest caution in applying this model to recently bottlenecked populations.     

Quantifying and managing the loss of genetic variation in a free-ranging population of takahe through the use of pedigrees

Pedigree analysis has clear benefits for the genetic management of threatened populations through the evaluation of inbreeding, population structure and genetic diversity. The use of pedigrees is usually restricted to captive populations and few examples exist of their exclusive use in managing free-ranging populations. One such example is the management of the takahe (Porphyrio hochstetteri), a highly endangered, flightless New Zealand rail at risk from introduced mammalian predators and habitat loss. During the 1980’s and 90’s, as part of the takahe recovery programme, birds were translocated from the sole remnant population in Fiordland to four offshore islands from which introduced predators had been eradicated. The subsequent “island” population, now numbering 83 and thought to be at carrying capacity, has been closely monitored since founding. Detailed breeding records allow us to analyse the island pedigree, which is up to 7 generations deep. Gene-drop analysis indicated that 7.5% of genetic diversity has been lost over the relatively short timeframe since founding (2.1 generations on average; total genetic founders = 31) due to both a failure to equalise founder representation early on and subsequent disproportionate breeding success (founder equivalents = 12.5; founder genome equivalents = 6.6). A high prevalence of close inbreeding will have also impacted on genetic diversity. Predictions from pedigree modelling suggest that 90% genetic diversity will be maintained for only 12 years, but by introducing a low level of immigration from the Fiordland population and permitting the population to grow, 90% GD could be maintained over the next 100 years. More generally, the results demonstrate the value of maintaining pedigrees for wild populations, especially in the years immediately after a translocation event.     

Genetic and morphometric diversity in Wallacea: geographical patterning in the horse shoe bat, Rhinolophus affinis

Genetic and morphometric variation was examined in eleven island populations of the horse‐shoe bat, Rhinolophus affinis, at the easterly end of this widespread species’ range and encompassing the Australian–Oriental biogeographic interface. Allozyme variation revealed mean heterozygosity levels within islands of 0.047, which is near the mammalian average. However, heterozygosity tended to decline from west to east as populations approached the periphery of the species’ distribution, and was lowest in those islands that were separated by the greatest sea‐crossing from source populations. There is extensive between‐island genetic differentiation (mean F_ST = 0.40) and relationships between islands are associated with their arrangement in geographical space; genetic distance is correlated with geographical distance and the genetic arrangement of islands is associated with longitude. The arrangement of islands as indicated by variation in body and skull metrics is also associated with their geographical positions, and the metric and genetic measures are themselves associated. While other taxa in the region have shown genetic‐geographical concordances, R. affinis is the only one that displays concordant patterns in metrical features. These patterns in biological diversity are interpreted as arising from the sequential island population structure and clines in key biogeographic gradients.     

Change in shoot proliferation with repeated in vitro subculture of shoots of woody species of Rosaceae

Shoots of 6 ornamental species and cultivars of Rosaceae were repeatedly subcultured in vitro for 9 generations on Linsmaier and Skoog (1965) medium with the addition of BA. Shoot proliferation increased over the first few generations and then gradually declined in all species and at all BA concentrations tested with the exception of Chaenomeles japonica in which a decline in shoot formation occurred only at 5.0 mg 1^-1 BA. A decrease in shoot length and leaf size and an increase in the incidence of callus formation was observed after several subcultures. This apparently irreversible decline could be due to either genetic or epigenetic change resulting from repeated fluxes in cytokinin, nutrient status or sucrose, or to elimination of seasonal environmental fluctuations.     

Invasion success of the bumblebee, Bombus terrestris, despite a drastic genetic bottleneck

In early 1992, the European bumblebee, Bombus terrestris, was first seen in Tasmania and currently has spread to most of the island. Here, we report on the genetic structure, using micro-satellites, of the invading population from samples collected in the years 1998-2000, a few years after the first sighting of the species in its new area. The data show that the Tasmanian population has a very low genetic diversity, with less than half of the allelic richness (Richness=2.89 alleles; H(exp)=0.591) and lower levels of heterozygosity as compared to populations in New Zealand (4.24 alleles; H(exp)=0.729) and Europe (5.08 alleles; H(exp)=0.826). In addition, the genetic data suggest that the invasion must have happened once, probably around late 1991, and was the result of very few, perhaps only two, individuals arriving in Tasmania. Furthermore, these founders came from the New Zealand population. Today, the population in the south of Tasmania seems to act as a source population from which individuals migrate into other parts of the state. A similar source-sink structure seems also the case for New Zealand. The data show that B. terrestris is a highly invasive species capable of establishing itself even after a dramatic genetic bottleneck. B. terrestris may be an invasive species due to the haplo-diploid sex determination system, which exposes recessive, deleterious mutations to selection. Offspring of such purged lines may then be able to tolerate high levels of inbreeding.     

Temporal dynamics of genetic variability in a mountain goat (Oreamnos americanus) population

The association between population dynamics and genetic variability is of fundamental importance for both evolutionary and conservation biology. We combined long-term population monitoring and molecular genetic data from 123 offspring and their parents at 28 microsatellite loci to investigate changes in genetic diversity over 14 cohorts in a small and relatively isolated population of mountain goats (Oreamnos americanus) during a period of demographic increase. Offspring heterozygosity decreased while parental genetic similarity and inbreeding coefficients (F(IS) ) increased over the study period (1995-2008). Immigrants introduced three novel alleles into the population and matings between residents and immigrants produced more heterozygous offspring than local crosses, suggesting that immigration can increase population genetic variability. The population experienced genetic drift over the study period, reflected by a reduced allelic richness over time and an 'isolation-by-time' pattern of genetic structure. The temporal decline of individual genetic diversity despite increasing population size probably resulted from a combination of genetic drift due to small effective population size, inbreeding and insufficient counterbalancing by immigration. This study highlights the importance of long-term genetic monitoring to understand how demographic processes influence temporal changes of genetic diversity in long-lived organisms.     

Rapid evolution of great kiskadees on Bermuda: an assessment of the ability of the island rule to predict the direction of contemporary evolution in exotic vertebrates

Aim To determine whether an exotic bird species, the great kiskadee (Pitangus sulphuratus), has diverged in morphology from its native source population, and, if so, has done so in a manner predicted by the island rule. The island rule predicts that insular vertebrates will tend towards dwarfism or gigantism when isolated on islands, depending on their body size. For birds, the island rule predicts that species with body sizes below 70–120 g should increase in size. The great kiskadee has a mean mass of c. 60 g in its native range, therefore we predicted that it would increase in size within the exotic, and more insular, Bermudan range. Location The islands of Bermuda (exotic population) and Trinidad (native source population). Methods We took eight morphological measurements on 84 individuals captured in the exotic (Bermudan) population and 62 individuals captured in the native source (Trinidadian) population. We compared morphological metrics between populations using univariate and principal components analyses. We assessed whether the effects of genetic drift could explain observed differences in morphology. We calculated divergence rates in haldanes and darwins for comparison with published examples of contemporary evolution. Finally, we used mark–recapture analysis to determine the effects of the measured morphological characters on survivorship within the exotic Bermudan population. Results Individuals in the exotic Bermudan population have larger morphological dimensions than individuals in the native source population on Trinidad. The degree of divergence in body mass (g) and bill width (mm) is probably not due to genetic drift. This rate of divergence is nearly equal to that observed amongst well‐documented examples of contemporary bird evolution, and is within the mid‐range of rates reported across taxa. There is no clear effect of body size on survivorship as only one character (bill width) was found to have an influence on individual survivorship. Main conclusions Exotic species provide useful systems for examining evolutionary predictions over contemporary time‐scales. We found that divergence between the exotic and native populations of this bird species occurred over c. 17 generations, and was in the direction predicted by the island rule, a principle based on the study of native species.     

Molecular genetic variation following a population crash in the endangered Mauna Kea silversword, Argyroxiphium sandwicense ssp. sandwicense (Asteraceae)

The endangered Mauna Kea silversword, Argyroxiphium sandwicense ssp. sandwicense (Asteraceae), has experienced a severe decline in distribution and abundance because of predation by alien ungulates. The small remnant natural population on the Mauna Kea volcano contains only 46 individuals. By contrast, the Haleakala silversword, A. sandwicense ssp. macrocephalum, consists of a large, vigorous population exceeding 60 000 individuals. Molecular genetic variation in the two populations was assessed using random amplified polymorphic DNA (RAPD) loci. Despite its severe crash in size, the Mauna Kea population did not differ significantly from the Haleakala population in the number of detectably polymorphic loci or in heterozygosity. The lack of substantial reduction in genetic variation, at least as measured with RAPD loci, suggests that the Mauna Kea population may not yet have gone through multiple generations at very small size.     

Gene flow and immigration rate in an island population of great tits

It is generally recognized that immigration and gene flow cannot be equated, but few detailed quantitative comparisons of these processes have been made over the entire lifetime of individual animals. We analyzed data collected in a longterm study of an island population of great tits Parus major, and tested two assumptions frequently made in population genetic studies. (1) The assumption that there is no difference in reproductive output between immigrant and resident breeding birds was refuted for females but not for males. Lifetime production of local recruits (LRS) was reduced by 37% in immigrant females, because female immigrants tended to leave the island after breeding, and thus reproduced for fewer years. Female LRS was density dependent, but the effect of density was independent of status (resident/immigrant). (2) The assumption that mating was random with respect to status was also refuted: assortative mating was found, even when temporal and spatial aggregation of immigrants was controlled for. Thus both assumptions were refuted, and gene flow was lower than immigration rate.     

Molecular Markers Allow to Remove Introgressed Genetic Background: A Simulation Study

The maintenance of genetically differentiated populations can be important for several reasons (whether for wild species or domestic breeds of economic interest). When those populations are introgressed by foreign individuals, methods to eliminate the exogenous alleles can be implemented to recover the native genetic background. This study used computer simulations to explore the usefulness of several molecular based diagnostic approaches to recover of a native population after suffering an introgression event where some exogenous alleles were admixed for a few generations. To remove the exogenous alleles, different types of molecular markers were used in order to decide which of the available individuals contributed descendants to next generation and their number of offspring. Recovery was most efficient using diagnostic markers (i.e., with private alleles) and least efficient when using alleles present in both native and exogenous populations at different frequencies. The increased inbreeding was a side-effect of the management strategy. Both values (% of native alleles and inbreeding) were largely dependent on the amount of exogenous individuals entering the population and the number of generations of admixture that occurred prior to management.     

Increase of heterozygosity in a growing population of lesser kestrels

The lesser kestrel (Falco naumanni) suffered a sharp population decline over much of its European distribution range in the middle of the twentieth century. Still declining in some areas, the species has recently experienced a notable population recovery in certain regions. We examined the genetic diversity variation in a growing population of lesser kestrels from Central Spain over a 6-year period (2000-2005). The population studied showed a rapid demographic expansion, increasing in the number of both breeding pairs and colonies. Annual average heterozygosity and allelic diversity increased and genetic similarity between potential mates decreased over the study period. Several immigrants regularly arrived in the study area and introduced new alleles into the local population, pointing to immigration as the main cause contributing to the observed genetic recovery.     

A population-genetic study of crab-eating macaques (Macaca fascicularis) on the island of Angaur, Palau, Micronesia

Blood protein polymorphisms of an introduced population of the crab-eating macaques on Angaur Island, Palau, Micronesia, were examined electrophoretically to assess genetic variability. Results showed a high degree of genetic heterozygosity and some distinctive features in the genetic constitution of this island population. Negative evidence is presented regarding ancestry from a single pair of macaques. Their origin is discussed in relation to the genetic structure of the present population.     

Genetic diversity and population size: island populations of the common shrew, Sorex araneus

Populations of many species are currently being fragmented and reduced by human interactions. These processes will tend to reduce genetic diversity within populations and reduce individual heterozygosities because of genetic drift, inbreeding and reduced migration. Conservation biologists need to know the effect of population size on genetic diversity, as this is likely to influence a population's ability to persist. Island populations represent an ideal natural experiment with which to study this problem. In a study of common shrews (Sorex araneus) on offshore Scottish islands, 497 individuals from 13 islands of different sizes and 6 regions on the mainland were trapped and genotyped at eight microsatellite loci. Previous genetic work had revealed that most of the islands in this study were highly genetically divergent from one another and the mainland. We found that most of the islands exhibited lower genetic diversity than the mainland populations. In the island populations, mean expected heterozygosity, mean observed heterozygosity and mean allelic richness were significantly positively correlated with log island size and log population size, which were estimated using habitat population density data and application of a Geographic Information System.     

Genetic diversity and population structure of an insular tree, Santalum austrocaledonicum in New Caledonian archipelago

We present a study of the genetic diversity and structure of a tropical tree in an insular system. Santalum austrocaledonicum is endemic to the archipelago of New Caledonia and is exploited for oil extraction from heartwood. A total of 431 individuals over 17 populations were analysed for eight polymorphic microsatellite loci. The number of alleles per locus ranged from 3 to 33 and the observed heterozygosity per population ranged from 0.01 in Mare to 0.74 in Ile des Pins. The genetic diversity was lowest in the most recent islands, the Loyautes, and highest in the oldest island, Grande Terre, as well as the nearby small Ile des Pins. Significant departures from panmixia were observed for some loci-population combinations (per population FIS = 0-0.03 on Grande-Terre and Ile des Pins, and 0-0.67 on Loyautes). A strong genetic differentiation among all islands was observed (FST = 0.22), and the amount of differentiation increased with geographic distance in Iles Loyaute and in Grande Terre. At both population and island levels, island age and isolation seem to be the main factors influencing the amount of genetic diversity. In particular, populations from recent islands had large average FIS that could not be entirely explained by null alleles or a Wahlund effect. This result suggests that, at least in some populations, selfing occurred extensively. Conclusively, our results indicate a strong influence of insularity on the genetic diversity and structure of Santalum austrocaledonicum.