Donald K. Price

Quantitative trait locus analyses and the study of evolutionary process

The past decade has seen a proliferation of studies that employ quantitative trait locus (QTL) approaches to diagnose the genetic basis of trait evolution. Advances in molecular techniques and analytical methods have suggested that an exact genetic description of the number and distribution of genes affecting a trait can be obtained. Although this possibility has met with some success in model systems such as Drosophila and Arabidopsis, the pursuit of an exact description of QTL effects, i.e. individual gene effect, in most cases has proven problematic. We discuss why QTL methods will have difficulty in identifying individual genes contributing to trait variation, and distinguish between the identification of QTL (or marker intervals) and the identification of individual genes or nucleotide differences within genes (QTN). This review focuses on what ecologists and evolutionary biologists working with natural populations can realistically expect to learn from QTL studies. We highlight representative issues in ecology and evolutionary biology and discuss the range of questions that can be addressed satisfactorily using QTL approaches. We specifically address developing approaches to QTL analysis in outbred populations, and discuss practical considerations of experimental (cross) design and application of different marker types. Throughout this review we attempt to provide a balanced description of the benefits of QTL methodology to studies in ecology and evolution as well as the inherent assumptions and limitations that may constrain its application.

Deciphering the routes of invasion of Drosophila suzukii by means of ABC random forest

Abstract Deciphering invasion routes from molecular data is crucial to understanding biological invasions, including identifying bottlenecks in population size and admixture among distinct populations. Here, we unravel the invasion routes of the invasive pest Drosophila suzukii using a multi-locus microsatellite dataset (25 loci on 23 worldwide sampling locations). To do this, we use approximate Bayesian computation (ABC), which has improved the reconstruction of invasion routes, but can be computationally expensive. We use our study to illustrate the use of a new, more efficient, ABC method, ABC random forest (ABC-RF) and compare it to a standard ABC method (ABC-LDA). We find that Japan emerges as the most probable source of the earliest recorded invasion into Hawaii. Southeast China and Hawaii together are the most probable sources of populations in western North America, which then in turn served as sources for those in eastern North America. European populations are genetically more homogeneous than North American populations, and their most probable source is northeast China, with evidence of limited gene flow from the eastern US as well. All introduced populations passed through bottlenecks, and analyses reveal five distinct admixture events. These findings can inform hypotheses concerning how this species evolved between different and independent source and invasive populations. Methodological comparisons indicate that ABC-RF and ABC-LDA show concordant results if ABC-LDA is based on a large number of simulated datasets but that ABC-RF out-performs ABC-LDA when using a comparable and more manageable number of simulated datasets, especially when analyzing complex introduction scenarios.

Potential use of low-copy nuclear genes in DNA barcoding: a comparison with plastid genes in two Hawaiian plant radiations

BackgroundDNA barcoding of land plants has relied traditionally on a small number of markers from the plastid genome. In contrast, low-copy nuclear genes have received little attention as DNA barcodes because of the absence of universal primers for PCR amplification.ResultsFrom pooled-species 454 transcriptome data we identified two variable intron-less nuclear loci for each of two species-rich genera of the Hawaiian flora: Clermontia (Campanulaceae) and Cyrtandra (Gesneriaceae) and compared their utility as DNA barcodes with that of plastid genes. We found that nuclear genes showed an overall greater variability, but also displayed a high level of heterozygosity, intraspecific variation, and retention of ancient alleles. Thus, nuclear genes displayed fewer species-diagnostic haplotypes compared to plastid genes and no interspecies gaps.ConclusionsThe apparently greater coalescence times of nuclear genes are likely to limit their utility as barcodes, as only a small proportion of their alleles were fixed and unique to individual species. In both groups, species-diagnostic markers from either genome were scarce on the youngest island; a minimum age of ca. two million years may be needed for a species flock to be barcoded. For young plant groups, nuclear genes may not be a superior alternative to slowly evolving plastid genes.

Rapid adaptive radiation and host plant conservation in the Hawaiian picture wing Drosophila (Diptera: Drosophilidae).

The Hawaiian picture wing Drosophila are a striking example of adaptive radiation in specialist saprophages on an island system. We use DNA sequences from five nuclear genes with a total of 4260 nucleotides to provide a comprehensive phylogeny and biogeographic analysis of 90 species in the Hawaiian Drosophila picture wing clade. The current analysis indicates that the evolution of the picture wing clade took place more recently than previously suggested. The relationships of several morphologically anomalous taxa are resolved with strong support. Biogeography and host plant analyses show two periods of rapid divergence occurred when Kauai and Oahu were the main high islands, indicating that a combination of complex topographical features of islands and development of novel host plant associations was key to the rapid diversification of these lineages. For the past 2 million years, host associations within lineages have been largely stable, and speciation has occurred primarily due to the establishment of populations on newer islands as they arose followed by divergence by isolation. The existence of several apparently relictual taxa suggests that extinction has also played a major role in assembly of the present Hawaiian Drosophila fauna.

Postharvest Irradiation Treatment for Quarantine Control of Drosophila suzukii (Diptera: Drosophilidae) in Fresh Commodities

ABSTRACT Irradiation is a postharvest quarantine treatment option for exported commodities such as stone fruits and small fruits to prevent movement of the new invasive pest spotted wing drosophila, Drosophila suzukii (Walker) (Diptera: Drosophilidae). The effects of irradiation on larval and pupal development and adult reproduction in D. suzukii were examined. Larvae (first, second, and third instars) and pupae (1-2-d-old, 3-5-d-old, and 7-8-d-old) on diet were irradiated at target doses of 20, 30, 40, and 50 Gy in replicated factorial experiments and survival to the adult stage was recorded. Tolerance to radiation increased with increasing age and developmental stage. Males and females were equally susceptible. A radiation dose of 40 Gy applied to first- and second-instar larvae prevented adult emergence. The late-stage pupa was the most radiation-tolerant stage that occurs in fruit, and individuals irradiated at this stage readily emerged as adults; therefore, prevention of F1 adults was the desired treatment response for large-scale validation tests with naturally infested fruit. In large-scale tests, a radiation dose of 80 Gy applied to late-stage pupae in sweet cherries or grapes resulted in no production of Fl adults in >33,000 treated individuals, which meets the zero tolerance requirement for market access. A minimum absorbed dose of 80 Gy is recommended for quarantine control of D. suzukii.

Gene discordance in phylogenomics of recent plant radiations, an example from Hawaiian Cyrtandra (Gesneriaceae).

Resolving species relationships within recent radiations requires analysis at the interface of phylogenetics and population genetics, where coalescence and hybridization may confound our understanding of relationships. We developed 18 new primer pairs for nuclear loci in Cyrtandra (Gesneriaceae), one of the largest plant radiations in the Pacific Islands, and tested the concordance of 14 loci in establishing the phylogenetic relationships of a small number of Hawaiian species. Four genes yielded tree topologies conflicting with the primary concordance tree, suggesting plastid capture and horizontal transfer via hybridization. Combining all concordant genes yielded a tree with stronger support and a different topology from the total-evidence tree. We conclude that a small number of genes may be insufficient for accurate reconstruction of the phylogenetic relationships among closely related species. Further, the combination of genes for phylogenetic analysis without preliminary concordance tests can yield an erroneous tree topology. It seems that the number of genes needed for phylogenetic analysis of closely related species is significantly greater than the small numbers commonly used, which fail to isolate coalescence, introgression and hybridization.

Genomic Signatures of Speciation in Sympatric and Allopatric Hawaiian Picture-Winged Drosophila.

The Hawaiian archipelago provides a natural arena for understanding adaptive radiation and speciation. The Hawaiian Drosophila are one of the most diverse endemic groups in Hawaiì with up to 1,000 species. We sequenced and analyzed entire genomes of recently diverged species of Hawaiian picture-winged Drosophila, Drosophila silvestris and Drosophila heteroneura from Hawaiì Island, in comparison with Drosophila planitibia, their sister species from Maui, a neighboring island where a common ancestor of all three had likely occurred. Genome-wide single nucleotide polymorphism patterns suggest the more recent origin of D. silvestris and D. heteroneura, as well as a pervasive influence of positive selection on divergence of the three species, with the signatures of positive selection more prominent in sympatry than allopatry. Positively selected genes were significantly enriched for functional terms related to sensory detection and mating, suggesting that sexual selection played an important role in speciation of these species. In particular, sequence variation in Olfactory receptor and Gustatory receptor genes seems to play a major role in adaptive radiation in Hawaiian pictured-winged Drosophila.

Physiological effects of heat stress on Hawaiian picture-wing Drosophila: genome-wide expression patterns and stress-related traits

Two Hawaiian picture-wing Drosophila differ in their temperature tolerances with the ecologically rare species, D. silvestris, showing reduced survival, reduced sperm mobility and greater gene expression changes at high temperatures compared to the common D. sproati. Thus the rare species may have reduced capacity to adapt to future climate changes.

Sexual Selection, Epistasis and Species Boundaries in Sympatric Hawaiian Picture-winged Drosophila

The Hawaiian picture-winged flies in the genus Drosophila are a spectacular example of rapid evolutionary diversification in which sexual selection is considered an important mechanism for reproductive isolation and speciation. We investigated the behavioral reproductive isolation of two closely related and sympatric Hawaiian picture-winged Drosophila species, D. silvestris and D. heteroneura, which are known to hybridize in nature and produce viable and fertile hybrids. We compared the mating success of parental, F1 and backcross males in pairings with D. heteroneura females. The F1 males were produced by mating D. heteroneura males with D. silvestris females, and the backcross males were produced by mating F1 females with D. heteroneura males. The mating success of backcross males paired with D. heteroneura females were significantly reduced relative to that of parental and F1 males. This reduced mating success occurred primarily at a late stage of courtship where female choice of mate may be important. Two- and three-gene models demonstrate that epistasis involving a few genes could account for the observed variation in male mating success. These results are consistent with negative epistasis in the backcross generation and support the importance of sexual selection and negative epistasis in the evolution and maintenance of these species.

A Test for Gene Flow among Sympatric and Allopatric Hawaiian Picture-Winged Drosophila

The Hawaiian Drosophila are one of the most species-rich endemic groups in Hawaii and a spectacular example of adaptive radiation. Drosophila silvestris and D. heteroneura are two closely related picture-winged Drosophila species that occur sympatrically on Hawaii Island and are known to hybridize in nature, yet exhibit highly divergent behavioral and morphological traits driven largely through sexual selection. Their closest-related allopatric species, D. planitibia from Maui, exhibits hybrid male sterility and reduced behavioral reproductive isolation when crossed experimentally with D. silvestris or D. heteroneura. A modified four-taxon test for gene flow was applied to recently obtained genomes of the three Hawaiian Drosophila species. The analysis indicates recent gene flow in sympatry, but also, although less extensive, between allopatric species. This study underscores the prevalence of gene flow, even in taxonomic groups considered classic examples of allopatric speciation on islands. The potential confounding effects of gene flow in phylogenetic and population genetics inference are discussed, as well as the implications for conservation.