Limited inbreeding depression in a bottlenecked population is age but not environment dependent

Inbreeding depression is known to vary greatly between populations and among species. Some of this variation is due to differences in genetic load between populations, while some is due to differences in the environment (e.g. local weather conditions) or demography of the population (e.g. age structure and breeding experience) in which inbreeding is expressed. Although the effects of these factors in isolation are well understood, there is still relatively little known about the interface between inbreeding on one hand, and environment and demography on the other in wild populations. We examined how environmental and demographic factors mediated the effects of inbreeding in a threatened species of bird. The Stewart Island robin, Petroica australis rakiura, has been subjected to a prolonged bottleneck for over 150 years. A complete pedigree of a reintroduced island population, extending back seven seasons to its founding, was available for analysis along with survival data (at the level of the brood) obtained from intensive monitoring over two breeding seasons. We found no strong support that the degree to which a brood was inbred affected its survival at either the hatching, fledging or recruitment stages. The inbreeding coefficient of the mother did have an effect on brood survival when analysed over all three life history stages, but only as a result of an interaction with female age, with broods of one‐year‐old inbred females suffering greater mortality than those of older inbred females. Although habitat type, temperature, rainfall and year were the best predictors of brood survival for most life history stages, their effects were weak and there were no interactions with inbreeding. Furthermore, there was no strong evidence of inbreeding depression associated with two periods of severe weather. This population is atypical in that inbreeding depression appears to be weak even under severe environmental conditions, and may be indicative that this bottlenecked population has either reduced genetic load or has fixed deleterious alleles.     

Genetic consequences of human management in an introduced island population of red deer (Cervus elaphus)

We investigated phylogeography and spatial genetic structure in an introduced island population of red deer (Cervus elaphus) on the Isle of Rum, Scotland, experiencing spatial variation in management regime. Five different mitochondrial DNA (mtDNA) haplotypes were present among female red deer on Rum. These comprised two phylogenetically divergent groups, one of which clustered with red deer from Sardinia and North Africa, while the other four grouped with other Western European red deer. Recent and historical red deer management practices explain this result. The Rum population is descended from recent introductions from at least four different UK mainland populations, and translocation of red deer within the UK and across Europe is well documented. We found significant spatial genetic structure across Rum in both mtDNA haplotypes and microsatellite markers. Mitochondrial spatial structure was over an order of magnitude greater than structure in nuclear markers. This extreme difference is explained by the fact that the Rum population was introduced from different source populations, the highly male-biased dispersal patterns of red deer and the much smaller effective population size of mitochondrial compared to nuclear markers. Spatial structure in mtDNA conformed to a pattern of isolation by distance, while nuclear DNA did not. Apparent structure in the nuclear markers was driven by differences between the North Block and the rest of the island. We suggest that recent differences in the management regimes in different parts of the island have led to differences in effective male migration that would account for this observation.     

Genetic conservation and management of the California endemic,Torrey pine (Pinus torreyana Parry): Implications of genetic rescue in a genetically depauperate species

Rare species present a challenge under changing environmental conditions as the genetic consequences of rarity may limit species ability to adapt to environmental change. To evaluate the evolutionary potential of a rare species, we assessed variation in traits important to plant fitness using multigenerational common garden experiments. Torrey pine, Pinus torreyana Parry, is one of the rarest pines in the world, restricted to one mainland and one island population. Morphological differentiation between island and mainland populations suggests adaptation to local environments may have contributed to trait variation. The distribution of phenotypic variances within the common garden suggests distinct population‐specific growth trajectories underlay genetic differences, with the island population exhibiting substantially reduced genetic variance for growth relative to the mainland population. Furthermore, F1 hybrids, representing a cross between mainland and island trees, exhibit increased height accumulation and fecundity relative to mainland and island parents. This may indicate genetic rescue via intraspecific hybridization could provide the necessary genetic variation to persist in environments modified as a result of climate change. Long‐term common garden experiments, such as these, provide invaluable resources to assess the distribution of genetic variance that may inform conservation strategies to preserve evolutionary potential of rare species, including genetic rescue.     

Genetic diversity does not explain variation in extra‐pair paternity in multiple populations of a songbird

Many songbirds are socially monogamous but genetically polyandrous, mating with individuals outside their pair bonds. Extra‐pair paternity (EPP) varies within and across species, but reasons for this variation remain unclear. One possible source of variation is population genetic diversity, which has been shown in interspecific meta‐analyses to correlate with EPP but which has limited support from intraspecific tests. Using eight populations of the genetically polyandrous red‐winged blackbird (Agelaius phoeniceus), including an island population, we investigated whether population‐level differences in genetic diversity led to differences in EPP. We first measured genetic diversity over 10 microsatellite loci and found, as predicted, low genetic diversity in the island population. Additional structure analyses with multilocus genotypes and mtDNA showed the island population to be distinct from the continental populations. However, the island population's EPP rate fell in the middle of the continental populations' distribution, whereas the continental populations themselves showed significant variation in EPP. This result suggests that genetic diversity by itself is not a predictor of EPP rate. We discuss reasons for the departure from previous results, including hypotheses for EPP that do not solely implicate female‐driven behaviour.     

Site-specific genetic divergence in parallel hybrid zones suggests nonallopatric evolution of reproductive barriers

The evolution of reproductive isolation in the presence of gene flow is supported by theoretical models but rarely by data. Empirical support might be gained from studies of parallel hybrid zones between interbreeding taxa. We analysed gene flow over two hybrid zones separating ecotypes of Littorina saxatilis to test the expectation that neutral genetic markers will show site-specific differences if barriers have evolved in situ. Distinct ecotypes found in contrasting shore habitats are separated by divergent selection and poor dispersal, but hybrid zones appear between them. Swedish islands formed by postglacial uplift 5000 years ago provide opportunities to assess genetic structure in a recently evolved system. Each island houses a discrete population containing subpopulations of different ecotypes. Hybrid zones between ecotypes may be a product of ecological divergence occurring on each island or a consequence of secondary overlap of ecotypes of allopatric origin that have spread among the islands. We used six microsatellite loci to assess gene flow and genetic profiles of hybrid zones on two islands. We found reduced gene flow over both hybrid zones, indicating the presence of local reproductive barriers between ecotypes. Nevertheless, subpopulations of different ecotypes from the same island were genetically more similar to each other than were subpopulations of the same ecotype from different islands. Moreover, neutral genetic traits separating the two ecotypes across hybrid zones were site-specific. This supports a scenario of in situ origin of ecotypes by ecological divergence and nonallopatric evolution of reproductive barriers.     

Differentiation with drift: a spatio-temporal genetic analysis of Galápagos mockingbird populations (Mimus spp.)

Small and isolated island populations provide ideal systems to study the effects of limited population size, genetic drift and gene flow on genetic diversity. We assessed genetic diversity within and differentiation among 19 mockingbird populations on 15 Galápagos islands, covering all four endemic species, using 16 microsatellite loci. We tested for signs of drift and gene flow, and used historic specimens to assess genetic change over the last century and to estimate effective population sizes. Within-population genetic diversity and effective population sizes varied substantially among island populations and correlated strongly with island size, suggesting that island size serves as a good predictor for effective population size. Genetic differentiation among populations was pronounced and increased with geographical distance. A century of genetic drift did not change genetic diversity on an archipelago-wide scale, but genetic drift led to loss of genetic diversity in small populations, especially in one of the two remaining populations of the endangered Floreana mockingbird. Unlike in other Galápagos bird species such as the Darwin''s finches, gene flow among mockingbird populations was low. The clear pattern of genetically distinct populations reflects the effects of genetic drift and suggests that Galápagos mockingbirds are evolving in relative isolation.     

Lost in transition--the Island of Susak (1951-2001)

The isolated population of the Island of Susak was thoroughly studied by a multidisciplinary team of the Croatian Academy of Sciences and Arts in early 1950's. Recently, a team of scientists revisited the island. This paper describes the main characteristics of the transition process during which a massive exodus occurred with 90% of the island's population migrating to New Jersey, USA. We summarise the differences in lifestyle, economy, social structure and sense of identity between the historic (1950's) and contemporary (2001) Susak population. We applied contemporary methods (analysis of microsatellite DNA polymorphisms) to investigate local myths about extreme levels of inbreeding and genetic homogeneity among the Susak islanders. Analysis of short-tandem-repeat (STR) loci showed that Susak displayed characteristics of a small homogeneous breeding isolate. The average heterozygosity was found to be low compared to outbred populations. The signature of a recent severe bottleneck could be detected. Analysis of 8 markers located on Xq13-21 in 71 individuals suggested extensive level of linkage disequilibrium (LD). A migrant study was designed to investigate the effects of large environmental changes (Susak vs. USA) and inbreeding (Susak vs. Croatian general population) on some biologically important quantitative traits, such as blood pressure and serum lipids. The results confirmed the positive correlation between inbreeding level and blood pressure that has been reported in the literature on several occasions. The last remnants of this traditional island community will soon be lost forever.     

Vicariance and marine migration in continental island populations of a frog endemic to the Atlantic Coastal forest

The theory of island biogeography is most often studied in the context of oceanic islands where all island inhabitants are descendants from founding events involving migration from mainland source populations. Far fewer studies have considered predictions of island biogeography in the case of continental islands, where island formation typically splits continuous populations and thus vicariance also contributes to the diversity of island populations. We examined one such case on continental islands in southeastern Brazil, to determine how classic island biogeography predictions and past vicariance explain the population genetic diversity of Thoropa taophora, a frog endemic to the Atlantic Coastal Forest. We used nuclear microsatellite markers to examine the genetic diversity of coastal and island populations of this species. We found that island isolation has a role in shaping the genetic diversity of continental island species, with island populations being significantly less diverse than coastal populations. However, area of the island and distance from coast had no significant effect on genetic diversity. We also found no significant differences between migration among coastal populations and migration to and from islands. We discuss how vicariance and the effects of continued migration between coastal and island populations interact to shape evolutionary patterns on continental islands.     

The dynamics of genetic and morphological variation on volcanic islands

Oceanic archipelagos of volcanic origin have been important in the study of evolution because they provide repeated natural experiments allowing rigorous tests of evolutionary hypotheses. Ongoing volcanism on these islands may, however, affect the evolutionary diversification of species. Analysis of population structure and phylogeographic patterns in island populations can provide insight into evolutionary dynamics on volcanic islands. We analysed genetic and morphological variation in the gecko Tarentola boettgeri on the island of Gran Canaria and compared it with Tarentola delalandii on Tenerife, a neighbouring volcanic island of similar age but distinctly different geological past. Intraspecific divergence of mitochondrial haplotypes indicates long-term persistence of Tarentola on each island, with a phylogeographic signal left by older volcanic events. More recent volcanic eruptions (approximately 0.2 million years ago on Tenerife, approximately 2.2 million years ago on Gran Canaria) have left a signature of population expansion in the population genetic structure, the strength of which depends on the time since the last major volcanic eruption on each island. While these stochastic events have left traces in morphological variation in Tenerife, in Gran Canaria geographical variation was solely associated with environmental variables. This suggests that historically caused patterns in morphology may be overwritten by natural selection within 2 million years.     

Historical range contraction,and not taxonomy,explains the contemporary genetic structure of the Australian tree <Emphasis Type="Italic">Acacia dealbata</Emphasis> Link

Irrespective of its causes, strong population genetic structure indicates a lack of gene flow. Understanding the processes that underlie such structure, and the spatial patterns it causes, is valuable for conservation efforts such as restoration. On the other hand, when a species is invasive outside its native range, such information can aid management in the non-native range. Here we explored the genetic characteristics of the Australian tree Acacia dealbata in its native range. Two subspecies of A. dealbata have previously been described based on morphology and environmental requirements, but recent phylogeographic data raised questions regarding the validity of this taxonomic subdivision. The species has been widely planted within and outside its native Australian range and is also a highly successful invasive species in many parts of the world. We employed microsatellite markers to investigate the population genetic diversity and structure among 42 A. dealbata populations from across the species’ native range. We also tested whether environmental variables purportedly relevant for the putative separation of subspecies are linked with population genetic differentiation. We found no relationship between population genetic structure of A. dealbata in Australia and these environmental features. Rather, we identified two geographically distinct genetic clusters that corresponded with populations in the northeastern part of mainland Australia, and the southern mainland and Tasmanian range of the species. Our results do not support the taxonomic subdivision of the species into two distinct subspecies based on environmental features. We therefore assume that the observed morphological differences between the putative subspecies are plastic phenotypic responses. This study provides population genetic information that will be useful for the conservation of the species within Australia as well as to better understand the invasion dynamics of A. dealbata.     

A molecular approach to understand the riddle of the invasive success of the tarantula,Brachypelma vagans,on Cozumel Island,Mexico

Invasive populations typically demonstrate genetic isolation which results in a loss of genetic diversity and a reduction in invasion success. This study focused on the genetic population of a successful invasive species of tarantula. Individuals were sampled in two mainland localities of the Yucatan Peninsula (Zoh-Laguna and Raudales), in addition to two island localities (El Cedral and Rancho Guadalupe on Cozumel Island). All populations present high genetic diversity (mean: H_e = 0.23, P = 99%), with significant differences between the Raudales and Rancho Guadalupe localities. The AMOVA analysis revealed a significant population structure (14.5% variation among populations), consistent with the gene differentiation coefficient (G_ST = 0.21), and spatial analysis of population structure. Our results suggested that the original introduced population did not suffer a loss of genetic diversity during establishment on the island, possibly a result of different biological conditions. Population structure analysis leads us to suggest that one island population is similar to the original genetic profile, whereas the genotypic profile of the other island population reflects recent introductions from the mainland. We identified a potential risk of extinction for one local mainland population, suggesting that this species may be a successful invader in a new environment but endangered in some parts of its natural area.     

Population Genetic Structure and Conservation of the Galápagos Petrel (Pterodroma phaeopygia)

The Galápagos petrel (Pterodroma phaeopygia) is endemic to the Galápagos archipelago, where it is known to breed only on five islands. The species has been listed as critically endangered due to habitat deterioration and predation by introduced mammals. Significant morphological and behavioural differences among petrels nesting on different islands suggest that island populations may differ genetically. Furthermore, nesting phenology suggests that genetically differentiated seasonal populations may exist within at least one island. We analysed variation in six microsatellite loci and part of the mitochondrial ATPase 6/8 gene in 206 Galápagos petrels sampled from all five islands. No evidence of genetic structuring within islands was found, although statistical power was low. In contrast, significant differences occurred among island populations. For the microsatellite loci, private alleles occurred at all islands, sometimes at high frequency; global and pairwise estimates of genetic differentiation were all statistically significant; Bayesian analysis of genotypes frequencies provided strong support for three genetic populations; and most estimates of migration between populations did not differ significantly from zero. Only two ATPase haplotypes were found, but the geographic distribution of haplotypes indicated significant differentiation among populations. For conservation purposes, populations from Floreana, Santa Cruz, San Cristóbal and Santiago should be regarded as separate genetic management units. Birds from Isabela appear to be derived recently from the Santiago population, and the population on San Cristóbal appears to be a mixture of birds from other populations. However, considering ecological and behavioural differences among birds from different islands, we recommend that all five populations be protected.     

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.     

The origin and genetic variability of the Czech sika deer population

Sika deer (Cervus nippon), native to Asia, formed two well-established free-living populations in the Czech Republic over the last century and continue to spread. Sika are also maintained in a large number of enclosures; these continue to introduce new individuals from the places of its origin as well as from other European countries. Despite extensive research into the morphology and ethology of the Czech sika deer, conducted over the last three decades, no study using genetic methods has been done. This study aimed to determine the genetic variability and the geographic origin of the Czech sika deer population. Two mitochondrial markers, the cytochrome b and the control region were analyzed in this study. Analysis of the two markers confirmed that the founder individuals of the Czech population originated from both native island (Japanese Islands) and native mainland (Far East Russia) populations. Results showed that the genetic variability of the Czech sika deer population is lower than the variability of the native Japanese population, but higher than that of the sampled part of the native Russian population. Also, the genetic variability was found to be higher within the samples from enclosures.     

When North and South don’t mix: genetic connectivity of a recently endangered oceanic cycad,Cycas micronesica,in Guam using EST‐microsatellites

Subject to environmental changes and recurrent isolation in the last ca. 250 Ma, cycads are often described as relicts of a previously common lineage, with populations characterized by low genetic variation and restricted gene flow. We found that on the island of Guam, the endemic Cycas micronesica has most of the genetic variation of 14 EST‐microsatellites distributed within each of 18 genetic populations, from 24 original sampling sites. There were high levels of genetic variation in terms of total number of alleles and private alleles, and moderate levels of inbreeding. Restricted but ongoing gene flow among populations within Guam reveals a genetic mosaic, probably more typical of cycads than previously assumed. Contiguous cycad populations in the north of Guam had higher self‐recruitment rates compared to fragmented populations in the south, with no substantial connection between them except for one population. Guam’s genetic mosaic may be explained by the influence of forest continuity, seed size, edaphic differences, and human transport of cycads. Also important are the extent of synchrony among flushes of reproductive female seed‐bearing sporophylls and restricted pollen movement by an obligate mutualist and generalist insects. An NADH EST‐locus under positive selection may reflect pressure from edaphic differences across Guam. This and three other loci are ideal candidates for ecological genomic studies. Given this species’ vulnerability due to the recent introduction of the cycad aulacaspis scale, we also identify priority populations for ex situ conservation, and provide a genetic baseline for understanding the effects of invasive species on cycads in the Western Pacific, and islands in general.     

Inter-island variation in femoral secretions of the Balearic lizard,Podarcis lilfordi (Lacertidae)

Many lizards use femoral gland secretions in intraspecific communication. Although there is a consistent interspecific variation in chemical composition of secretions, considerable variation is also often found between populations, which may affect conspecifc recognition and lead to speciation processes. Balearic lizards (Podarcis lilfordi) are currently distributed only in several isolated islets offshore of the main islands with different environmental conditions (vegetation, diet, density of population, etc). Also, there is a high genetic variability between populations. We examined whether there was a similar variation in the composition of the femoral secretions of male lizards, and which could be the causes of such variation. By using GC–MS analyses, we found 75 lipophilic compounds in femoral gland secretions of male P. lilfordi from three representative island populations. Main compounds were steroids (94.4%), mainly cholesterol, but we also found alkanes, ketones, waxy esters, squalene, carboxylic acids and their ethyl esters, alcohols and other minor compounds. However, there were clear differences between populations with respect to the number and relative proportions of compounds. Using the patterns of presence and abundance of compounds in secretions it is possible to predict the population of origin of a lizard. We discuss how these differences could be explained considering genetic and environmental differences between populations.     

Philopatry drives genetic differentiation in an island archipelago: comparative population genetics of Galapagos Nazca boobies (Sula granti) and great frigatebirds (Fregata minor)

Seabirds are considered highly mobile, able to fly great distances with few apparent barriers to dispersal. However, it is often the case that seabird populations exhibit strong population genetic structure despite their potential vagility. Here we show that Galapagos Nazca booby (Sula granti) populations are substantially differentiated, even within the small geographic scale of this archipelago. On the other hand, Galapagos great frigatebird (Fregata minor) populations do not show any genetic structure. We characterized the genetic differentiation by sampling five colonies of both species in the Galapagos archipelago and analyzing eight microsatellite loci and three mitochondrial genes. Using an F‐statistic approach on the multilocus data, we found significant differentiation between nearly all island pairs of Nazca booby populations and a Bayesian clustering analysis provided support for three distinct genetic clusters. Mitochondrial DNA showed less differentiation of Nazca booby colonies; only Nazca boobies from the island of Darwin were significantly differentiated from individuals throughout the rest of the archipelago. Great frigatebird populations showed little to no evidence for genetic differentiation at the same scale. Only two island pairs (Darwin – Wolf, N. Seymour – Wolf) were significantly differentiated using the multilocus data, and only two island pairs had statistically significant φ_ST values (N. Seymour – Darwin, N. Seymour – Wolf) according to the mitochondrial data. There was no significant pattern of isolation by distance for either species calculated using both markers. Seven of the ten Nazca booby migration rates calculated between island pairs were in the south or southeast to north or northwest direction. The population differentiation found among Galapagos Nazca booby colonies, but not great frigatebird colonies, is most likely due to differences in natal and breeding philopatry.     

An experimental test of the causes of small-scale phenotypic differentiation in a population of great tits

Phenotypic differentiation between populations is thought to occur mainly at spatial scales where gene-flow is restricted and selection regimes differ. However, if gene flow is nonrandom, dispersal may reinforce, rather than counteract, evolutionary differentiation, meaning that differences occurring over small scales might have a genetic basis. The purpose of this study was to determine the cause of differences in mean phenotype between two parts of a population of great tits Parus major, separated by <3 km. We conducted a partial cross-fostering experiment between two contrasting parts of this population to separate genetic and environmental sources of variation, and to test for gene-environment interaction. We found strong environmental effects on nestling size, mass and condition index, with nestlings reared in a low density part of the population being larger, heavier and in better condition, than those in a high density part, irrespective of their origin. In addition, we found smaller, but significant, differences in nestling condition and shape associated with the areas that birds originated from, suggesting the presence of genetic differences between parts of this population. There was no evidence of gene-environment interaction for any character. This experiment is thus consistent with previous analyses suggesting that differences between parts of this population had evolved recently, apparently due to phenotype-dependent dispersal, and indicates that population differentiation can be maintained over small spatial scales despite extensive dispersal.     

Cancer incidence in eastern Adriatic isolates, Croatia: examples from the islands of Krk, Cres, Losinj, Rab and Pag

As an extension of previous research this study investigates the incidence of cancer in five genetic isolate island populations of the Eastern Adriatic, Croatia. Thorough anthropological research over the past three decades has established some of those populations as outstanding examples of genetic isolates. A previous study which found higher cancer incidence in 5 Eastern Adriatic islands than in a control population supported a hypothesis that among the founders of these populations there were genetic variants (especially with recessive inheritance) responsible for genetic susceptibility to certain types of cancer. This study sought to investigate cancer incidence in 5 further island populations. All cancer cases in five island populations (Krk, Cres, Losinj, Rab and Pag) over the 20-year period (1971 to 1990) was extracted from the data of the Croatian Cancer Registry. The mainland populations of Istrian and Primorsko-Goranska County, characterized by similar environmental factors but an outbred genetic structure, represented a control population. After standardization by by sex and age, cancer incidence was higher in the island populations than in the control population in both sexes. The cancer sites primarily responsible for the excess incidence were prostate, stomach and pancreatic cancer in males, and ovarian, breast, stomach, bowel, and brain cancer in females. The reasons for the increased cancer incidence are uncertain and may be due to different environmental exposure between the two populations. However, it is possible that genetic isolation and inbreeding are important factors. Further investigations of cancer in these isolate populations are warranted to explore these findings further.