GENETIC MODELS OF ADAPTATION AND GENE FLOW IN PERIPHERAL POPULATIONS

We investigate the interplay between gene flow and adaptation in peripheral populations of a widespread species. Models are developed for the evolution of a quantitative trait under clinally varying selection in a species whose density decreases from the center of the range to its periphery. Two major results emerge. First, gene flow from populations at the range center can be a strong force that inhibits peripheral populations from evolving to their local ecological optima. As a result, peripheral populations experience persistent directional selection. Second, response to local selection pressures can cause rapid and substantial evolution when a peripheral population is isolated from gene flow. The amount of evolutionary change depends on gene flow, selection, the ecological gradient, and the trait's heritability. Rapid divergence can also occur between the two halves of a formerly continuous population that is divided by a vicariant event. A general conclusion is that disruption of gene flow can cause evolutionary divergence, perhaps leading to speciation, in the absence of contributions from random genetic drift.     

QUANTITATIVE GENETIC DIVERGENCE AND STANDING GENETIC (CO)VARIANCE IN THERMAL REACTION NORMS ALONG LATITUDE

Although the potential to adapt to warmer climate is constrained by genetic trade‐offs, our understanding of how selection and mutation shape genetic (co)variances in thermal reaction norms is poor. Using 71 isofemale lines of the fly Sepsis punctum, originating from northern, central, and southern European climates, we tested for divergence in juvenile development rate across latitude at five experimental temperatures. To investigate effects of evolutionary history in different climates on standing genetic variation in reaction norms, we further compared genetic (co)variances between regions. Flies were reared on either high or low food resources to explore the role of energy acquisition in determining genetic trade‐offs between different temperatures. Although the latter had only weak effects on the strength and sign of genetic correlations, genetic architecture differed significantly between climatic regions, implying that evolution of reaction norms proceeds via different trajectories at high latitude versus low latitude in this system. Accordingly, regional genetic architecture was correlated to region‐specific differentiation. Moreover, hot development temperatures were associated with low genetic variance and stronger genetic correlations compared to cooler temperatures. We discuss the evolutionary potential of thermal reaction norms in light of their underlying genetic architectures, evolutionary histories, and the materialization of trade‐offs in natural environments.     

GENETIC DIVERGENCE ALONG THE SPECIATION CONTINUUM: THE TRANSITION FROM HOST RACE TO SPECIES IN RHAGOLETIS (DIPTERA: TEPHRITIDAE)

Studies of related populations varying in their degrees of reproductive isolation can provide insights into speciation. Here, the transition from partially isolated host races to more fully separated sibling species is investigated by comparing patterns of genetic differentiation between recently evolved (～150 generations) apple and ancestral hawthorn‐infesting populations of Rhagoletis pomonella to their sister taxon, the undescribed flowering dogwood fly attacking Cornus florida. No fixed or diagnostic private alleles differentiating the three populations were found at any of 23 microsatellites and 10 allozymes scored. Nevertheless, allele frequency differences were sufficient across loci for flowering dogwood fly populations from multiple localities to form a diagnosable genotypic cluster distinct from apple and hawthorn flies, indicative of species status. Genome‐wide patterns of differentiation were correlated between the host races and species pair comparisons along the majority of chromosomes, suggesting that similar disruptive selection pressures affect most loci. However, differentiation was more pronounced, with some additional regions showing elevated divergence, for the species pair comparison. Our results imply that Rhagoletis sibling species such as the flowering dogwood fly represent host races writ large, with the transition to species status primarily resulting from increased divergence of the same regions separating apple and hawthorn flies.     

EVOLVABILITY OF INDIVIDUAL TRAITS IN A MULTIVARIATE CONTEXT: PARTITIONING THE ADDITIVE GENETIC VARIANCE INTO COMMON AND SPECIFIC COMPONENTS

Genetic covariation among multiple traits will bias the direction of evolution. Although a trait's phenotypic context is crucial for understanding evolutionary constraints, the evolutionary potential of one (focal) trait, rather than the whole phenotype, is often of interest. The extent to which a focal trait can evolve independently depends on how much of the genetic variance in that trait is unique. Here, we present a hypothesis‐testing framework for estimating the genetic variance in a focal trait that is independent of variance in other traits. We illustrate our analytical approach using two Drosophila bunnanda trait sets: a contact pheromone system comprised of cuticular hydrocarbons (CHCs), and wing shape, characterized by relative warps of vein position coordinates. Only 9% of the additive genetic variation in CHCs was trait specific, suggesting individual traits are unlikely to evolve independently. In contrast, most (72%) of the additive genetic variance in wing shape was trait specific, suggesting relative warp representations of wing shape could evolve independently. The identification of genetic variance in focal traits that is independent of other traits provides a way of studying the evolvability of individual traits within the broader context of the multivariate phenotype.     

MAJOR GENETIC DIFFERENCES BETWEEN CROWN-OF-THORNS STARFISH (ACANTHASTER PLANCI) POPULATIONS IN THE INDIAN AND PACIFIC OCEANS

Spatial variation in allelic frequencies at nine allozyme loci were assayed in 20 populations of the crown-of-thorns starfish, Acanthaster planci, collected throughout the Pacific and Indian Oceans. These data were analyzed together with published data, for the same loci, from an additional 19 populations, giving a total sample size of approximately 1800 individuals. There was a marked discontinuity between the Indian and Pacific Ocean populations, but those off Western Australia and from the Southeast Asian region had a strong Pacific affinity. The genetic groups were congruent with the distributions of two color morph groups: gray-green to red-brown forms in the Pacific and a blue to pale red form in the Indian Ocean. These patterns of genetic structure are similar to those described for the starfish Linckia laevigata, which has similar life-history characteristics. Vicariant events may have influenced some populations within the Pacific, but the allozyme data cannot resolve the effects of these events clearly. Patterns of variation within regions were consistent with isolation by distance, but, at larger scales, were obscured by regional vicariance and some outliers, particularly by apparently high levels of gene flow between Japan and the Great Barrier Reef, Australia. Apparent gene flow between population pairs was not closely related to present-day ocean currents. The results demonstrate a strong influence of allopatric separation on genetic divergence at large geographic scales, but also show evidence of slow rates of change in gene frequencies consistent with the large population sizes of this species. Low levels of divergence between groups demonstrate the genetic structure is recent (Pleistocene) and are likely responses to changes in climate and sea level.     

POPULATION STRUCTURE OF DIPODOMYS INGENS (HETEROMYIDAE): THE ROLE OF SPATIAL HETEROGENEITY IN MAINTAINING GENETIC DIVERSITY

The giant kangaroo rat, Dipodomys ingens (Heteromyidae), is an endangered rodent that inhabits approximately 3% of its estimated historic range. Its current distribution is centered in two geographic areas, situated about 150 km apart, in south-central California. We sequenced a 293 base-pair fragment at the 5' end of the control region in 95 giant kangaroo rats from nine localities to examine the genetic structure of extant populations. We determine that mutations in this section of the control region follow a negative binominal distribution, rather than a Poisson. However, the distance between haplotypes is small enough that the difference between a tree that corrects for the non-Poisson distribution of mutations and one that does not, is minimal. This implies that the use of methods that assume a Poisson distribution of mutations, such as those based on coalescent theory, are justified. We find that the correlation between levels of genetic diversity and estimated census size is poor. This suggests that population sizes have fluctuated over time or that populations have not been isolated from one another, or both. We also examine the hierarchical structure of populations and find that the southern populations are not genetically subdivided but that there is significant subdivision between northern and southern populations and between some northern subpopulations. The phylogeographic relationship between northern and southern populations can primarily be attributed to isolation by distance, although the time since divergence between them appears to be less than the age of either. To examine the phylogeographic relationships in more detail we construct a minimum spanning tree based on Tamura-Nei gamma-corrected distances and superimpose on it the geographic position of haplotypes. This reveals that there is more genetic distance between some northern haplotypes than between any northern and southern haplotypes, despite the geographic distance separating north from south and the larger size of the southern population. It also reveals that one northern population, in the Panoche Valley, contains old allelic lineages and shares ancestral polymorphism with several other populations. It also shows that two, small, geographically remote populations contain a surprising amount of genetic diversity, but that different population/geographic processes have affected the structure of that diversity. We estimate the average migration rate among all populations to be 7.5 per generation, and conclude that a disproportionate number of migration events involve gene flow with one northern population, the Panoche Valley. We find evidence for the hypothesis that there has been an increase in population size in the remaining populations in the north and suggest that the Panoche Valley could play a role in these expansions. Finally we discuss the probabilitiy that the genetic structure of the southern populations has been affected by fluctuations in size. These results are briefly compared to other studies on the genetic structure of rodent populations.     

MOLECULAR GENETIC ANALYSIS OF A STEPPED MULTILOCUS CLINE IN THE AMERICAN OYSTER (CRASSOSTREA VIRGINICA)

Gulf of Mexico versus Atlantic populations of several coastal species in the southeastern United States are known to differ sharply in genetic composition, but most transitional zones have not previously been examined in detail. Here we employ molecular markers from mitochondrial and nuclear loci to characterize cytonuclear genetic associations at meso- and microgeographic scales along an eastern Florida transitional zone between genetically distinct Atlantic and Gulf populations of the American oyster, Crassostrea virginica. The single- and multilocus cytonuclear patterns display: (1) a cline extending along 340 km of the east Florida coastline; (2) a pronounced step in the cline centered at Cape Canaveral (shifts in allelic frequencies by 50–75% over a 20 km distance); (3) a close agreement of observed genotypic frequencies with Hardy-Weinberg expectations within locales; and (4) mild or nonexistent nuclear and cytonuclear disequilibria in most local population samples. These results imply: (1) considerable restrictions to interpopulational gene flow along the eastern Florida coastline; (2) within locales, free interbreeding (as opposed to mere population admixture) between Gulf and Atlantic forms of oysters; and (3) localized population recruitment in the transition zone localities. These findings demonstrate that marine organisms with high dispersal potential via long-lived pelagic larvae can nonetheless display pronounced spatial population genetic structure, and more generally they exemplify the utility of pronounced genetic transition zones for the study of population level processes.     

THE GENETIC ARCHITECTURE OF REPRODUCTIVE ISOLATION DURING SPECIATION‐WITH‐GENE‐FLOW IN LAKE WHITEFISH SPECIES PAIRS ASSESSED BY RAD SEQUENCING

During speciation‐with‐gene‐flow, effective migration varies across the genome as a function of several factors, including proximity of selected loci, recombination rate, strength of selection, and number of selected loci. Genome scans may provide better empirical understanding of the genome‐wide patterns of genetic differentiation, especially if the variance due to the previously mentioned factors is partitioned. In North American lake whitefish (Coregonus clupeaformis), glacial lineages that diverged in allopatry about 60,000 years ago and came into contact 12,000 years ago have independently evolved in several lakes into two sympatric species pairs (a normal benthic and a dwarf limnetic). Variable degrees of reproductive isolation between species pairs across lakes offer a continuum of genetic and phenotypic divergence associated with adaptation to distinct ecological niches. To disentangle the complex array of genetically based barriers that locally reduce the effective migration rate between whitefish species pairs, we compared genome‐wide patterns of divergence across five lakes distributed along this divergence continuum. Using restriction site associated DNA (RAD) sequencing, we combined genetic mapping and population genetics approaches to identify genomic regions resistant to introgression and derive empirical measures of the barrier strength as a function of recombination distance. We found that the size of the genomic islands of differentiation was influenced by the joint effects of linkage disequilibrium maintained by selection on many loci, the strength of ecological niche divergence, as well as demographic characteristics unique to each lake. Partial parallelism in divergent genomic regions likely reflected the combined effects of polygenic adaptation from standing variation and independent changes in the genetic architecture of postzygotic isolation. This study illustrates how integrating genetic mapping and population genomics of multiple sympatric species pairs provide a window on the speciation‐with‐gene‐flow mechanism.     

MICROSATELLITE MARKERS REVEAL POPULATION GENETIC STRUCTURE OF THE TOXIC DINOFLAGELLATE ALEXANDRIUM TAMARENSE (DINOPHYCEAE) IN JAPANESE COASTAL WATERS1

This is the first report to explore the fine‐scale diversity, population genetic structure, and biogeography of a typical planktonic microbe in Japanese and Korean coastal waters and also to try to detect the impact of natural and human‐assisted dispersals on the genetic structure and gene flow in a toxic dinoflagellate species. Here we present the genetic analysis of Alexandrium tamarense (Lebour) Balech populations from 10 sites along the Japanese and Korean coasts. We used nine microsatellite loci, which varied widely in number of alleles and gene diversity across populations. The analysis revealed that Nei's genetic distance correlated significantly with geographic distance in pair‐wise comparisons, and that there was genetic differentiation in about half of 45 pair‐wise populations. These results clearly indicate genetic isolation among populations according to geographic distance and restricted gene flow via natural dispersal through tidal currents among the populations. On the other hand, high P‐values in Fisher's combined test were detected in five pair‐wise populations, suggesting similar genetic structure and a close genetic relationship between the populations. These findings suggest that the genetic structure of Japanese A. tamarense populations has been disturbed, possibly by human‐assisted dispersal, which has resulted in gene flow between geographically separated populations.     

HIERARCHICAL SPATIAL STRUCTURE AND DISCRIMINANT ANALYSIS OF GENETIC DIVERSITY IN THE RED ALGA MAZZAELLA LAMINARIOIDES (GIGARTINALES, RHODOPHYTA)

Our study of the genetic structure of Mazzaella laminarioides (Bory) Fredericq (Gigartinales) in the central Chilean region documented a high level of genetic diversity based on random amplified polymorphic DNA (RAPD) markers and indicated the occurrence of significant genetic structure at different spatial scales. A total of 288 haploid gametophytes was analyzed with 17 polymorphic RAPD bands, which produced 202 distinct multilocus genotypes. Within stands, mean gene diversity ranged from 0.210 to 0.249 and no significant linkage disequilibrium could be detected among pairs of alleles, revealing that recombination (sexual reproduction) regularly shuffles the genes at that scale. Analysis of molecular variance within stands (less than 30 m) showed that the structure was very low, only marginally significant, and did not increase with increasing hierarchical levels at this lowest spatial scale. In contrast, at a larger spatial scale (among stands, from 5 to 60 km), increasing geographical distance seemed to account for increasing isolation between populations even if natural barriers, such as sandy beaches or river estuaries, may play a role in such isolation. Moreover, the strong genetic differentiation occurring between locations separated by 60 km allowed the assignment of individuals to their original population through a canonical discriminant analysis. This approach further allowed the identification of potential recent migrants from one population to the other. Thus, in species like M. laminarioides for which the dominance of RAPD markers can be avoided by selecting haploid individuals, RAPD analysis appeared to be specially appropriate for the study of genetic differentiation.     

GENETIC STRUCTURE OF GIANT CLAM (TRIDACNA MAXIMA) POPULATIONS IN THE WEST PACIFIC IS NOT CONSISTENT WITH DISPERSAL BY PRESENT-DAY OCEAN CURRENTS

The Pacific marine biota, particularly species with long planktonic larval stages, are thought to disperse widely throughout the Pacific via ocean currents. The little genetic data available to date has supported this view in that little or no significant regional differentiation of populations has been found over large geographical distances. However, recent data from giant clams has demonstrated not only significant regional differentiation of populations, but routes of gene flow that run perpendicular to the main present-day ocean currents. Extensive surveys of genetic variation at eight polymorphic loci in 19 populations of the giant clam Tridacna maxima, sampled throughout the West and Central Pacific, confirmed that the patterns of variation seen so far in T. gigas were not unique to that species, and may reflect a fundamental genetic structuring of shallow-water marine taxa. Populations of T. maxima within highly connected reef systems like the Great Barrier Reef were panmictic (average F_ST < 0.003), but highly significant genetic differences between reef groups on different archipelagos (average F_ST = 0.084) and between West and Central Pacific regions (average F_ST = 0.156) were found. Inferred gene flow was high (N_em usually > 5) between the Philippines and the Great Barrier Reef, between the Philippines and Melanesia (the Solomon Islands and Fiji), and between the Philippines and the Central Pacific island groups (Marshall Islands, Kiribati, Tuvalu and Cook Islands). Gene flow was low between these three sets of island chains (N_em < 2). These routes of gene flow are perpendicular to present-day ocean currents. It is suggested that the spatial patterns of gene frequencies reflect past episodes of dispersal at times of lower sea levels which have not been erased by subsequent dispersal by present-day circulation. The patterns are consistent with extensive dispersal of marine species in the Pacific, and with traditional views of dispersal from the Indo-Malay region. However, they demonstrate that dispersal along present-day ocean surface currents cannot be assumed, that other mechanisms may operate today or that major dispersal events are intermittent (perhaps separated by several thousands of years), and that the nature and timing of dispersal of Pacific marine species is more complex than has been thought.     

SPECIATION IN THE EUROPEAN RABBIT (ORYCTOLAGUS CUNICULUS): ISLANDS OF DIFFERENTIATION ON THE X CHROMOSOME AND AUTOSOMES

Studies of gene flow between closely related taxa can provide insight into the genetic basis of speciation. To evaluate the importance of the X chromosome in reproductive isolation between subspecies of the European rabbit and to study the genomic scale over which islands of differentiation extend, we resequenced a total of 34 loci distributed along the X chromosome and chromosome 14. Previous studies based on few markers suggested that loci in centromeric regions were highly differentiated between rabbit subspecies, whereas loci in telomeric regions were less differentiated. Here, we confirmed this finding but also discovered remarkable variation in levels of differentiation among loci, with F_ST values from nearly 0 to 1. Analyses using isolation‐with‐migration models suggest that this range appears to be largely explained by differential levels of gene flow among loci. The X chromosome was significantly more differentiated than the autosomes. On chromosome 14, differentiation decayed very rapidly at increasing distances from the centromere, but on the X chromosome distinct islands of differentiation encompassing several megabases were observed both at the centromeric region and along the chromosome arms. These findings support the idea that the X chromosome plays an important role in reproductive isolation between rabbit subspecies. These results also demonstrate the mosaic nature of the genome at species boundaries.     

GENETIC POPULATION STRUCTURE AND LEVELS OF GENE FLOW IN THE STREAM DWELLING WATERSTRIDER,AQUARIUS (=GERRIS) REMIGIS (HEMIPTERA: GERRIDAE)

Gene flow, in combination with selection and drift, determines levels of differentiation among local populations. In this study we estimate gene flow in a stream dwelling, flightless waterstrider, Aquarius remigis. Twenty-eight Aquarius remigis populations from Quebec, Ontario, New Brunswick, Iowa, North Carolina, and California were genetically characterized at 15 loci using starch gel electrophoresis. Sampling over two years was designed for a hierarchical analysis of population structure incorporating variation among sites within streams, streams within watersheds, watersheds within regions, and regions within North America. Hierarchical F statistics indicated that only sites within streams maintained enough gene flow to prevent differentiation through drift (Nm = 27.5). Above the level of sites within streams gene flow is highly restricted (Nm ≤ 0.5) and no correlation is found between genetic and geographic distances. This agrees well with direct estimates of gene flow based on mark and recapture data, yielding an N_e of approximately 170 individuals. Previous assignment of subspecific status to Californian A. remigis is not supported by genetic distances between those populations and other populations in North America. Previous suggestion of specific status for south-eastern A. remigis is supported by genetic distances between North Carolina populations and other populations in North America, and a high proportion of region specific alleles in the North Carolina populations. However, because of the high degree of morphological and genetic variability throughout the range of this species, the assignment of specific or subspecific status to parts of the range may be premature.