Localizing F(ST) outliers on a QTL map reveals evidence for large genomic regions of reduced gene exchange during speciation-with-gene-flow.

Populations that maintain phenotypic divergence in sympatry typically show a mosaic pattern of genomic divergence, requiring a corresponding mosaic of genomic isolation (reduced gene flow). However, mechanisms that could produce the genomic isolation required for divergence-with-gene-flow have barely been explored, apart from the traditional localized effects of selection and reduced recombination near centromeres or inversions. By localizing F(ST) outliers from a genome scan of wild pea aphid host races on a Quantitative Trait Locus (QTL) map of key traits, we test the hypothesis that between-population recombination and gene exchange are reduced over large 'divergence hitchhiking' (DH) regions.

Population genetic structure and secondary symbionts in host-associated populations of the pea aphid complex.

Polyphagous insect herbivores experience different selection pressures on their various host plant species. How this affects population divergence and speciation may be influenced by the bacterial endosymbionts that many harbor. Here, we study the population structure and symbiont community of the pea aphid (Acyrthosiphon pisum), which feeds on a range of legume species and is known to form genetically differentiated host-adapted populations.

Divergence hitchhiking and the spread of genomic isolation during ecological speciation-with-gene-flow.

In allopatric populations, geographical separation simultaneously isolates the entire genome, allowing genetic divergence to accumulate virtually anywhere in the genome. In sympatric populations, however, the strong divergent selection required to overcome migration produces a genetic mosaic of divergent and non-divergent genomic regions. In some recent genome scans, each divergent genomic region has been interpreted as an independent incidence of migration/selection balance, such that the reduction of gene exchange is restricted to a few kilobases around each divergently selected gene.

Natural selection in action during speciation.

The role of natural selection in speciation, first described by Darwin, has finally been widely accepted. Yet, the nature and time course of the genetic changes that result in speciation remain mysterious. To date, genetic analyses of speciation have focused almost exclusively on retrospective analyses of reproductive isolation between species or subspecies and on hybrid sterility or inviability rather than on ecologically based barriers to gene flow.

The genetic mosaic suggests a new role for hitchhiking in ecological speciation.

Early in ecological speciation, the genomically localized effects of divergent selection cause heterogeneity among loci in divergence between incipient species. We call this pattern of genomic variability in divergence the 'genetic mosaic of speciation'. Previous studies have used F(ST) outliers as a way to identify divergently selected genomic regions, but the nature of the relationship between outlier loci and quantitative trait loci (QTL) involved in reproductive isolation has not yet been quantified.

The genetic architecture of ecological specialization: correlated gene effects on host use and habitat choice in pea aphids.

Genetic correlations among phenotypic characters result when two traits are influenced by the same genes or sets of genes. By reducing the degree to which traits in two environments can evolve independently (e.g.

The ecological genetics of speciation.

Ecological interactions and the natural selection they cause play a prominent causal role in biological diversification and speciation. As a discipline, ecological genetics integrates the two components of adaptive evolution (natural selection and genetic variability) to study the mechanisms of evolution. Ecological genetics is a fruitful approach to the study of how reproductive isolation can evolve under natural selection.

Population differentiation and genetic variation in performance on eight hosts in the pea aphid complex.

Phytophagous insects frequently use multiple host-plant species leading to the evolution of specialized host-adapted populations and sometimes eventually to speciation. Some insects are confronted with a large number of host-plant species, which may provide complex routes of gene flow between host-adapted populations. The pea aphid (Acyrthosiphon pisum) attacks a broad range of plants in the Fabaceae and it is known that populations on Trifolium pratense and Medicago sativa can be highly specialized at exploiting these species.

Population differentiation and genetic variation in host choice among pea aphids from eight host plant genera.

Habitat choice plays a critical role in the processes of host range evolution, specialization, and ecological speciation. Pea aphid, Acyrthosiphon pisum, populations from alfalfa and red clover in eastern North America are known to be genetically differentiated and show genetic preferences for the appropriate host plant. This species feeds on many more hosts, and here we report a study of the genetic variation in host plant preference within and between pea aphid populations collected from eight genera of host plants in southeastern England.

Back to the future: genetic correlations, adaptation and speciation.

Genetic correlations can affect the course of phenotypic evolution. Although genetic correlations among traits are a common feature of quantitative genetic analyses, they have played a very minor role in recent linkage-map based analyses of the genetic architecture of quantitative traits. Here, we use our work on host-associated races in pea aphids to illustrate how quantitative trait locus (QTL) mapping can be used to test specific hypotheses about how genetic correlations may facilitate ecological specialization and speciation.

Specialized Feeding Behavior Influences Both Ecological Specialization and Assortative Mating in Sympatric Host Races of Pea Aphids.

Not only is ecological specialization a defining feature of much of Earth's biological diversity, the evolution of specialization may also play a central role in generating diversity by facilitating speciation. To understand how ecological specialization evolves, we must know the particular characters that cause organisms to be specialized. For example, most theories of specialization in herbivorous insects emphasize physiological trade-offs in response to toxic plant chemicals.

REPRODUCTIVE ISOLATION BETWEEN SYMPATRIC RACES OF PEA APHIDS. I. GENE FLOW RESTRICTION AND HABITAT CHOICE.

Determining the extent and causes of barriers to gene flow between genetically divergent populations or races of single species is an important complement to post facto analyses of the causes of reproductive isolation between recognized species. Sympatric populations of pea aphids (Acyrthosiphon pisum Harris, Homoptera: Aphididae) on alfalfa and red clover are highly genetically divergent and locally adapted. Here, hierarchical estimates of population structure based on F suggest that gene exchange between closely adjacent aphid populations on the two hosts is highly restricted relative to that among fields of the same host plant.

EVOLUTION OF AN APHID-PARASITOID INTERACTION: VARIATION IN RESISTANCE TO PARASITISM AMONG APHID POPULATIONS SPECIALIZED ON DIFFERENT PLANTS.

The evolution of associations between herbivorous insects and their parasitoids is likely to be influenced by the relationship between the herbivore and its host plants. If populations of specialized herbivorous insects are structured by their host plants such that populations on different hosts are genetically differentiated, then the traits affecting insect-parasitoid interactions may exhibit an associated structure. The pea aphid (Acyrthosiphon pisum) is a herbivorous insect species comprised of genetically distinct groups that are specialized on different host plants (Via 1991a, 1994).

SHORT-TERM EVOLUTION IN THE SIZE AND SHAPE OF PEA APHIDS.

Phenotypic evolution in contemporary populations can generally be witnessed only when novel selective forces produce rapid evolution. Examples of conditions that have led to rapid evolution include drastic environmental change, invasion of a new predator, or a host-range expansion. In cyclical parthenogens, however, yearly cycles of phenotypic evolution may occur due to the loss of adaptation during recombination in the sexual phase (genetic slippage), permitting an opportunity to observe adaptive evolutionary change in contemporary populations that are not necessarily subject to new patterns of natural selection.

THE POTENTIAL FOR COEVOLUTION IN A HOST-PARASITOID SYSTEM. I. GENETIC VARIATION WITHIN AN APHID POPULATION IN SUSCEPTIBILITY TO A PARASITIC WASP.

For coevolution to occur, there must be genetic variation in each species for traits relevant to their interaction. Here, statistically significant variation in susceptibility to a parasitic wasp was found among pea-aphid clones collected from a single population. In a subset of clones that was tested further, wasps were found to oviposit in aphids from both resistant and susceptible lines, but eggs failed to develop in resistant hosts.

THE GENETIC STRUCTURE OF HOST PLANT ADAPTATION IN A SPATIAL PATCHWORK: DEMOGRAPHIC VARIABILITY AMONG RECIPROCALLY TRANSPLANTED PEA APHID CLONES.

Populations of insect herbivores that feed on several host plant species may experience different selective forces on each host. When the hosts cooccur in a local area, herbivore populations can provide useful models for the study of evolutionary mechanisms in patchy environments. A first step in such a study involves determination of the genetic structure of host adaptation in the region: how is genetic variation for host use structured within and between subpopulations of herbivores on each host? The structure of genetic variation for host use reveals patterns of local adaptation, probable selective consequences of migration between hosts, and the potential for further evolution.

GENETIC COVARIANCE BETWEEN OVIPOSITION PREFERENCE AND LARVAL PERFORMANCE IN AN INSECT HERBIVORE.

An experimental study determined that females of the herbivorous fly species Liriomyza sativae (Diptera: Agromyzidae) preferentially oviposit on the plant species on which their female progeny attain the greatest pupal weight. A modified parent/offspring regression was used to quantify this relationship as an additive genetic covariance between host-plant preference and relative performance of female larvae on different plant species. The implications of a genetic covariance between preference and performance on the course of evolution in herbivores are discussed.

GENOTYPE-ENVIRONMENT INTERACTION AND THE EVOLUTION OF PHENOTYPIC PLASTICITY.

Studies of spatial variation in the environment have primarily focused on how genetic variation can be maintained. Many one-locus genetic models have addressed this issue, but, for several reasons, these models are not directly applicable to quantitative (polygenic) traits. One reason is that for continuously varying characters, the evolution of the mean phenotype expressed in different environments (the norm of reaction) is also of interest.

THE ONTOGENY AND SPECTRAL SENSITIVITY OF POLAROTAXIS IN LARVAE OF THE CRAB RHITHROPANOPEUS HARRISI (GOULD).

1. To determine the ontogeny plus the intensity and spectral characteristics of polarotaxis in larvae of the crab, Rhithropanopeus harrisi, swimming paths in relation to the e-vector direction of linearly polarized light were monitored and recorded with a closed circuit video system. 2.