Genetic and phylogenetic consequences of island biogeography

Abstract.— Island biogeography theory predicts that the number of species on an island should increase with island size and decrease with island distance to the mainland. These predictions are generally well supported in comparative and experimental studies. These ecological, equilibrium predictions arise as a result of colonization and extinction processes. Because colonization and extinction are also important processes in evolution, we develop methods to test evolutionary predictions of island biogeography. We derive a population genetic model of island biogeography that incorporates island colonization, migration of individuals from the mainland, and extinction of island populations. The model provides a means of estimating the rates of migration and extinction from population genetic data. This model predicts that within an island population the distribution of genetic divergences with respect to the mainland source population should be bimodal, with much of the divergence dating to the colonization event. Across islands, this model predicts that populations on large islands should be on average more genetically divergent from mainland source populations than those on small islands. Likewise, populations on distant islands should be more divergent than those on close islands. Published observations of a larger proportion of endemic species on large and distant islands support these predictions.     

Growth and body weight of European hares in southern Sweden

Body weight and growth of European hares Lepus europaeus Pallas in relation to environmental conditions, population density, age, sex, and reproduction were studied in three populations in southern Sweden on the basis of hares shot during October-December. There were no significant differences in mean body weight of juveniles in the three areas. Differences in juvenile growth, as indicated by the correlation between eye lens weight (age indicator) and body weight, between areas and years were related to variations in nutrient conditions, in an island population it was probably also related to population density. Adult body weights did not differ between two mainland areas despite differences in food supply and population density, whereas island adult hares were, on average, significantly lighter than mainland hares. Also this difference was ascribed to nutrient conditions and/or population density. There were no significant differences in body weight between adult hares of different age classes. But reproductive females showed a significant positive correlation between number of litters produced annually and body weight. This relation indicates that reproduction is favoured by large body size and body weight, which also might explain the average higher mean body weight in females than in males. Juvenile hares showed no clear tendency in sex dimorphism of body weight.     

Comparison of life-history characteristics of island and mainland populations of the swamp antechinus

The reproductive ecology of the swamp antechinus Antechinus minimus , a small dasyurid (Dasyuridae) marsupial with obligate male semelparity, was investigated in populations inhabiting the mainland coast and on a nearby offshore island in south-eastern Australia. The size and sex ratios of litters, individual body mass and size, timing of births and female longevity were determined from live-trapped animals. The island population had significantly smaller litter sizes and greater adult body mass in comparison with the mainland population. This is consistent with features of the 'island syndrome', which predicts directional selection for these traits in high-density populations with reduced extrinsic mortality. However, inter-annual variability in litter sizes in the island population suggests that litter size is more responsive to fluctuating local conditions, such as population density, which is likely to affect food availability, rather than directional genetic changes. In contrast with other antechinus species, biased sex ratios were not evident. In addition, large variations of the timing of births were estimated at both sites and these appear to be related to seasonal conditions such as autumn rainfall and female body mass before mating.     

Genetic variation and structure of house sparrow populations: is there an island effect?

Population genetic structure and intrapopulation levels of genetic variation have important implications for population dynamics and evolutionary processes. Habitat fragmentation is one of the major threats to biodiversity. It leads to smaller population sizes and reduced gene flow between populations and will thus also affect genetic structure. We use a natural system of island and mainland populations of house sparrows along the coast of Norway to characterize the different population genetic properties of fragmented populations. We genotyped 636 individuals distributed across 14 populations at 15 microsatellite loci. The level of genetic differentiation was estimated using F‐statistics and specially designed Mantel tests were conducted to study the influence of population type (i.e. mainland or island) and geographic distance on the genetic population structure. Furthermore, the effects of population type, population size and latitude on the level of genetic variation within populations were examined. Our results suggest that genetic processes on islands and mainland differed in two important ways. First, the intrapopulation level of genetic variation tended to be lower and the occurrence of population bottlenecks more frequent on islands than the mainland. Second, although the general level of genetic differentiation was low to moderate, it was higher between island populations than between mainland populations. However, differentiation increased in mainland populations somewhat faster with geographical distance. These results suggest that population bottleneck events and genetic drift have been more important in shaping the genetic composition of island populations compared with populations on the mainland. Such knowledge is relevant for a better understanding of evolutionary processes and conservation of threatened populations.     

An example of phenotypic adherence to the island rule? – Anticosti gray jays are heavier but not structurally larger than mainland conspecifics

The island rule refers to the tendency of small vertebrates to become larger when isolated on islands and the frequent dwarfing of large forms. It implies genetic control, and a necessary linkage, of size and body‐mass differences between insular and mainland populations. To examine the island rule, we compared body size and mass of gray jays (Perisoreus canadensis) on Anticosti Island, Québec, located in the Gulf of St. Lawrence, with three mainland populations (2 in Québec and 1 in Ontario). Although gray jays on Anticosti Island were ca 10% heavier, they were not structurally larger, than the three mainland populations. This suggests that Anticosti jays are not necessarily genetically distinct from mainland gray jays and that they may have achieved their greater body masses solely through packing more mass onto mainland‐sized body frames. As such, they may be the first‐known example of a proposed, purely phenotypic initial step in the adherence to the island rule by an insular population. Greater jay body mass is probably advantageous in Anticosti's high‐density, intensely competitive social environment that may have resulted from the island's lack of mammalian nest predators.     

Genetic variation and island biogreography: Microsatellite and mitochondrial DNA variation in island populations of the Australian bush rat, Rattus fuscipes greyii

To understand the impact of various factors on the maintenance of genetic variation in natural populations, we need to focus on situations where at least some of these factors are removed or controlled. In this study, we used highly variable, presumably neutral, microsatellite and mtDNA markers to assess the nature of genetic variation in 14 island and two mainland populations of the Australian bush rat, where there is no migration between islands. Thus we are controlling for selection and gene flow. Both marker sets revealed low levels of diversity within the small island populations and extreme differentiation between populations. For six microsatellite loci, all of the small island populations had less genetic variation than the mainland populations; reduction in allelic diversity was more pronounced than loss of heterozygosity. Kangaroo Island, the large island population, had similar levels of diversity to the mainland populations. A 442 base pair (bp) section of the mtDNA control region was screened for variation by outgroup heteroduplex analysis/temperature gradient gel electrophoresis (OHA/TGGE). Only three of the 13 small island populations showed haplotypic diversity: Gambier (2), Waldegrave (2), and Eyere (3). The level of haplotypic diversity in the small island populations was similar to that on the mainland, most likely reflecting a recent population bottleneck on the mainland. In contrast, Kangaroo Island had 9 mtDNA haplotypes. The dominant factor influencing genetic diversity on the islands was island size. No correlation was detected between genetic diversity and the time since isolation or distance form the mainland. The combination of genetic drift within and complete isolation among the small island populations has resulted in rapid and extreme population divergence. Population pair-wise comparisons of allele frequency distributions showed significant differences for all populations for all loci (F _st = 0.11–0.84, R _st = 0.07–0.99). For the mtDNA control region, 92.6% of variation was apportioned between populations; only the Pearson islands shared a haplotype. Mantel tests of pair-wise genetic distance with pair-wise geographic distance showed no significant geographical clustering of haplotypes. However, population substructuring was detected within populations where sampling was conducted over a broader geographical range, as indicated by departures from Hardy-Weinberg equilibrium. Thus substructuring in the ancestral population cannot be ruled out. The dominant evolutionary forces on the islands, after the initial founder event, are stochastic population processes such as genetic drift and mutation. This revised version was published online in July 2006 with corrections to the Cover Date.     

Allozyme variation at a PGI locus in differently aged populations of Moehringia trinervia (Caryophyllaceae) in a successional area

We studied genetic effects of the colonisation process during primary succession by analysing allozyme variation at a PGI locus in differently aged populations of Moehringia trinervia , which is a selfing annual with low dispersal ability. The populations studied come from islands and shores created in the 1880s by a drop in the water table of a Swedish lake and from old parts of a large island and of the mainland. The population age is known from five vegetation analyses over a century. We have also analysed the genetic composition of M. trinervia derived from seeds in the soil. Mainland populations had a higher genetic diversity than island populations that were little differentiated and differed genetically from the mainland populations. There was no temporal trend in the distribution of genetic variation on the new islands. The presence of alleles in the extant populations was associated with the proportion of that allele in the seed bank, indicating a main recruitment from the seed bank and not by repeated immigrations. We suggest that some of the new islands were colonised by a few early founders from the mainland. Later colonisation has occurred between adjacent islands, which preserves the founder effect and could explain the uniform, low genetic variation in the island populations.     

Evolutionary history of Scinax treefrogs on land‐bridge islands in south‐eastern Brazil

Aim We investigated how Pleistocene refugia and recent (c. 12,000 years ago) sea level incursions shaped genetic differentiation in mainland and island populations of the Scinax perpusillus treefrog group. Location Brazilian Atlantic Forest, São Paulo state, south‐eastern Brazil. Methods Using mitochondrial and microsatellite loci, we examined population structure and genetic diversity in three species from the S. perpusillus group, sampled from three land‐bridge islands and five mainland populations, in order to understand the roles of Pleistocene forest fragmentation and sea level incursions on genetic differentiation. We calculated metrics of relatedness and genetic diversity to assess whether island populations exhibit signatures of genetic drift and isolation. Two of the three island populations in this study have previously been described as new species based on a combination of distinct morphological and behavioural characters, thus we used the molecular datasets to determine whether phenotypic change is consistent with genetic differentiation. Results Our analyses recovered three distinct lineages or demes composed of northern mainland São Paulo populations, southern mainland São Paulo populations, and one divergent island population. The two remaining island populations clustered with samples from adjacent mainland populations. Estimates of allelic richness were significantly lower, and estimates of relatedness were significantly higher, in island populations relative to their mainland counterparts. Main conclusions Fine‐scale genetic structure across mainland populations indicates the possible existence of local refugia within São Paulo state, underscoring the small geographic scale at which populations diverge in this species‐rich region of the Atlantic Coastal Forest. Variation in genetic signatures across the three islands indicates that the populations experienced different demographic processes after marine incursions fragmented the distribution of the S. perpusillus group. Genetic signatures of inbreeding and drift in some island populations indicate that small population sizes, coupled with strong ecological selection, may be important evolutionary forces driving speciation on land‐bridge islands.     

Large mainland populations of South Island robins retain greater genetic diversity than offshore island refuges

For conservation purposes islands are considered safe refuges for many species, particularly in regions where introduced predators form a major threat to the native fauna, but island populations are also known to possess low levels of genetic diversity. The New Zealand archipelago provides an ideal system to compare genetic diversity of large mainland populations where introduced predators are common, to that of smaller offshore islands, which serve as predator-free refuges. We assessed microsatellite variation in South Island robins (Petroica australis australis), and compared large mainland, small mainland, natural island and translocated island populations. Large mainland populations exhibited more polymorphic loci and higher number of alleles than small mainland and natural island populations. Genetic variation did not differ between natural and translocated island populations, even though one of the translocated populations was established with five individuals. Hatching failure was recorded in a subset of the populations and found to be significantly higher in translocated populations than in a large mainland population. Significant population differentiation was largely based on heterogeneity in allele frequencies (including fixation of alleles), as few unique alleles were observed. This study shows that large mainland populations retain higher levels of genetic diversity than natural and translocated island populations. It highlights the importance of protecting these mainland populations and using them as a source for new translocations. In the future, these populations may become extremely valuable for species conservation if existing island populations become adversely affected by low levels of genetic variation and do not persist.     

Genetic drift and rapid evolution of viviparity in insular fire salamanders (Salamandra salamandra)

Continental islands offer an excellent opportunity to investigate adaptive processes and to time microevolutionary changes that precede macroevolutionary events. We performed a population genetic study of the fire salamander (Salamandra salamandra), a species that displays unique intraspecific diversity of reproductive strategies, to address the microevolutionary processes leading to phenotypic and genetic differentiation of island, coastal and interior populations. We used eight microsatellite markers to estimate genetic diversity, population structure and demographic parameters in viviparous insular populations and ovoviviparous coastal and interior populations. Our results show considerable genetic differentiation (F(ST) range: 0.06-0.27), and no clear signs of gene flow among populations, except between the large and admixed interior populations. We find no support for island colonization by rafting or intentional/accidental anthropogenic introductions, indicating that rising sea levels were responsible for isolation of the island populations approximately 9000 years ago. Our study provides evidence of rapid genetic differentiation between island and coastal populations, and rapid evolution of viviparity driven by climatic selective pressures on island populations, geographic isolation with genetic drift, or a combination of these factors. Studies of these viviparous island populations in early stages of divergence help us better understand the microevolutionary processes involved in rapid phenotypic shifts.     

Larger body size on islands affects silvereye Zosterops lateralis song and call frequency

Differences in song repertoires and characteristics of island and mainland populations of the same avian species are usually explained by dispersal, cultural evolution and/or habitat differences. The influence of morphology is often overlooked, even though island populations are frequently morphologically distinct from mainland populations, and morphology could affect vocalizations. I compared morphological features, songs, contact calls and alarm calls of six isolated island populations of silvereye Zosterops lateralis with those of two mainland populations to examine whether differences between mainland and island vocalizations were consistent across vocalization types, and whether these differences could be linked to morphological differences. Vocalizations were lower in frequency on islands. Island individuals were larger (both in mass and body structure), and body mass was an important predictor of frequency in contact and alarm calls. I argue that this strong association results from the island rule (islands promote larger body sizes) and cascading effects of morphology on vocalization frequency in this species.     

Reduced MHC class II diversity in island compared to mainland populations of the black-footed rock-wallaby (<Emphasis Type="Italic">Petrogale lateralis lateralis</Emphasis>)

Many animal populations that are endangered in mainland areas exist in stable island populations, which have the potential to act as an “ark” in case of mainland population declines. Previous studies have found neutral genetic variation in such species to be up to an order of magnitude lower in island compared to mainland populations. If low genetic variation is prevalent across fitness-related loci, this would reduce the effectiveness of island populations as a source of individuals to supplement declining mainland populations or re-establish extinct mainland populations. One such species, the black-footed rock-wallaby (Petrogale lateralis lateralis), exists within fragmented mainland populations and small island populations off Western Australia. We examined sequence variation in this species within a fitness-related locus under positive selection, the MHC class II DAB β1 locus. The mainland populations displayed greater levels of allelic diversity (4–7 alleles) than the island population, despite being small and isolated, and contained at least two DAB gene copies. The island population displayed low allelic diversity (2 alleles) and fewer alleles per individual in comparison to mainland populations, and probably possesses only one DAB gene copy. The patterns of DAB diversity suggested that the island population has a markedly lower level of genetic variation than the mainland populations, in concordance with results from microsatellites (genotyped in a previous study), but preserved unique alleles which were not found in mainland populations. Where possible, conservation actions should pool individuals from multiple populations, not only island populations, for translocation programs, and focus on preventing further declines in mainland populations.     

Population size and time since island isolation determine genetic diversity loss in insular frog populations

Understanding the factors that contribute to loss of genetic diversity in fragmented populations is crucial for conservation measurements. Land‐bridge archipelagoes offer ideal model systems for identifying the long‐term effects of these factors on genetic variations in wild populations. In this study, we used nine microsatellite markers to quantify genetic diversity and differentiation of 810 pond frogs (Pelophylax nigromaculatus) from 24 islands of the Zhoushan Archipelago and three sites on nearby mainland China and estimated the effects of the island area, population size, time since island isolation, distance to the mainland and distance to the nearest larger island on reduced genetic diversity of insular populations. The mainland populations displayed higher genetic diversity than insular populations. Genetic differentiations and no obvious gene flow were detected among the frog populations on the islands. Hierarchical partitioning analysis showed that only time since island isolation (square‐root‐transformed) and population size (log‐transformed) significantly contributed to insular genetic diversity. These results suggest that decreased genetic diversity and genetic differentiations among insular populations may have been caused by random genetic drift following isolation by rising sea levels during the Holocene. The results provide strong evidence for a relationship between retained genetic diversity and population size and time since island isolation for pond frogs on the islands, consistent with the prediction of the neutral theory for finite populations. Our study highlights the importance of the size and estimated isolation time of populations in understanding the mechanisms of genetic diversity loss and differentiation in fragmented wild populations.     

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.     

Evolutionary effects of geographic and climatic isolation between Rhododendron tsusiophyllum populations on the Izu Islands and mainland Honshu of Japan

Geographic and environmental isolations of islands and the mainland offer excellent opportunity to investigate colonization and survival dynamics of island populations. We inferred and compared evolutionary processes and the demographic history of Rhododendron tsusiophyllum, in the Izu Islands and the much larger island Honshu, treated here as the mainland, using thousands of nuclear SNPs obtained by ddRAD-seq from eight populations of R. tsusiophyllum and three populations of R. tschonoskii as an outgroup. Phylogenetic relationships and their habitats suggest that R. tsusiophyllum had evolved and migrated from cold north to warm south regions. We detected clear genetic divergence among populations in three regions of Honshu and the Izu Islands, suggesting restricted migration between them due to isolated habitats on mountains even in the mainland. The three regions have different changes in effective population size, especially, genetic diversity and population size of the Izu Islands are small compared to the others. Further, habitats of populations in the Izu Islands are warmer than those in Honshu, suggesting that they have undergone adaptive evolution. Our study provides evidences of montane rather than insular isolation on genetic divergence, survival of populations and significance of adaptive evolution for island populations with small population size and low genetic diversity, despite close proximity to mainland populations.Subject terms: Genetic variation, Plant evolution, Conservation biology     

Genetic differentiation between Apis cerana cerana populations from Damen Island and adjacent mainland in China

Geographic isolation interrupted gene flow between populations leading to population differentiation during the long evolutionary period. In this paper, 33 colonies from Damen Island and 100 colonies from adjacent mainland populations, Juxi and Chixi, were analyzed with both mitochondrial tRNA^leu-COII sequences and five microsatellite loci. The results showed that Apis cerana cerana population from Damen Island significantly differentiated from its adjacent mainland populations. In addition, Damen Island population showed a lower level of genetic diversity in terms of the number of mitochondrial haplotypes while both island and mainland populations showed a low level of genetic diversity with mutilocus analysis. The divergent small island population A.c. cerana might probably have suffered inbreeding and genetic drift as well as limited gene flow across the strait. Our data provides useful information for management and preservation for the Damen Island population.     

Dwarfism in insular sloths: biogeography,selection, and evolutionary rate

The islands of Bocas del Toro, Panama, were sequentially separated from the adjacent mainland by rising sea levels during the past 10,000 years. Three-toed sloths (Bradypus) from five islands are smaller than their mainland counterparts, and the insular populations themselves vary in mean body size. We first examine relationships between body size and physical characteristics of the islands, testing hypotheses regarding optimal body size, evolutionary equilibria, and the presence of dispersal in this system. To do so, we conduct linear regressions of body size onto island area, distance from the mainland, and island age. Second, we retroactively calculate two measures of the evolutionary rate of change in body size (haldanes and darwins) and the standardized linear selection differential, or selection intensity (i). We also test the observed morphological changes against models of evolution by genetic drift. The results indicate that mean body size decreases linearly with island age, explaining up to 97% of the variation among population means. Neither island area nor distance from the mainland is significant in multiple regressions that include island age. Thus, we find no evidence for differential optimal body size among islands, or for dispersal in the system. In contrast, the dependence of body size on island age suggests uniform directional selection for small body size in the insular populations. Although genetic drift cannot be discounted as the cause for this evolution in body size, the probability is small given the consistent direction of evolution (repeated dwarfism). The insular sloths show a sustained rate of evolution similar to those measured in haldanes over tens of generations, appearing to unite micro- and macroevolutionary time scales. Furthermore, the magnitude and rate of this example of rapid differentiation fall within predictions of theoretical models from population genetics. However, the linearity of the relationship between body size and island age is not predicted, suggesting that either more factors are involved than those considered here, or that theoretical advances are necessary to explain constant evolutionary rates over long time spans in new selective environments.     

COLOR-PATTERN VARIATION IN LAKE ERIE WATER SNAKES: THE ROLE OF GENE FLOW

In an effort to clarify the evolutionary processes influencing color-pattern variation in Lake Erie island water snake (Nerodia sipedon) populations, rates of gene flow among island and mainland populations were estimated from patterns of allozymic variation detected using electrophoresis. Rates of gene flow were high with Nm, the number of migrants per generation, averaging 25.5 among island sites, 9.2 between the Ontario mainland and the islands, and 3.6 between the Ohio mainland and the islands. Based on estimates of current population size from mark-recapture work and of past population size extrapolated from the extent of shoreline habitat, values of m between island and mainland populations ranged from 0.0008–0.01. Synthesis of estimates of the rate of gene flow with information on inheritance of color pattern, the strength of natural selection, and population history supports the hypothesis that color-pattern variation in island populations results from a balance between gene flow and natural selection. However, depending on the mode of inheritance of color pattern, stochastic processes such as drift may have been important in the initial stages of differentiation between island and mainland populations.     

Reproduction in the European hare in southern Sweden

Reproduction in the European hare Lepus europaeus Pallas populations was studied in three study areas in South Sweden during 1974–1976; two on the mainland and the third on the Island of Ven in Öresund. The monthly birth rates was calculated on the basis of the age of juvenile hares shot in autumn. The first births always occurred in February, indicating that the onset of the breeding season was governed by day length rather than by climate. Later, the reproduction rate was determined by temperature, snow cover, and precipitation. Low temperatures in spring delayed the reproduction; high temperatures in autumn favoured a prolongation of the breeding season. Low precipitation in May-July caused a decline in reproduction in July in a sandy pasture area, mainly because water amount was low in the green forage. Annual fertility, estimated on the basis of placental scars, varied between 6.8 and 8.9 young per female. There was a significant negative correlation between fertility and population density. The largest variations were recorded in one-year-old females, and on average the values were significantly higher in three-year-old females. 68% of all females examined had three litters annually; four litters were found in only 13% of all females. The mean litter size for the whole period was about 2.9 in all areas. The size of the first litter was significantly higher in females producing one or two litters than in females with three or four litters. The postnatal losses were on average 30–35% lower in the island population than in the mainland populations (73–84%), probably due to lack of predators, sparse road traffic, and inhibited juvenile dispersal.     

Convergence in reduced body size,head size,and blood glucose in three island reptiles

Many oceanic islands harbor diverse species that differ markedly from their mainland relatives with respect to morphology, behavior, and physiology. A particularly common morphological change exhibited by a wide range of species on islands worldwide involves either a reduction in body size, termed island dwarfism, or an increase in body size, termed island gigantism. While numerous instances of dwarfism and gigantism have been well documented, documentation of other morphological changes on islands remains limited. Furthermore, we lack a basic understanding of the physiological mechanisms that underlie these changes, and whether they are convergent. A major hypothesis for the repeated evolution of dwarfism posits selection for smaller, more efficient body sizes in the context of low resource availability. Under this hypothesis, we would expect the physiological mechanisms known to be downregulated in model organisms exhibiting small body sizes due to dietary restriction or artificial selection would also be downregulated in wild species exhibiting dwarfism on islands. We measured body size, relative head size, and circulating blood glucose in three species of reptiles—two snakes and one lizard—in the California Channel Islands relative to mainland populations. Collating data from 6 years of study, we found that relative to mainland population the island populations had smaller body size (i.e., island dwarfism), smaller head sizes relative to body size, and lower levels of blood glucose, although with some variation by sex and year. These findings suggest that the island populations of these three species have independently evolved convergent physiological changes (lower glucose set point) corresponding to convergent changes in morphology that are consistent with a scenario of reduced resource availability and/or changes in prey size on the islands. This provides a powerful system to further investigate ecological, physiological, and genetic variables to elucidate the mechanisms underlying convergent changes in life history on islands.