A continuum of genetic divergence from sympatric host races to species in the pea aphid complex

Abstract

Sympatric populations of insects adapted to different host plants, i.e., host races, are good models to investigate how natural selection can promote speciation in the face of ongoing gene flow. However, host races are documented in very few model systems and their gradual evolution into good species, as assumed under a Darwinian view of species formation, lacks strong empirical support. We aim at resolving this uncertainty by investigating host specialization and gene flow among populations of the pea aphid complex, Acyrthosiphon pisum. Genetic markers and tests of host plant specificity indicate the existence of at least 11 well-distinguished sympatric populations associated with different host plants in Western Europe. Population assignment tests show variable migration and hybridization rates among sympatric populations, delineating 8 host races and 3 possible species. Notably, hybridization correlates negatively with genetic differentiation, forming a continuum of population divergence toward virtually complete speciation. The pea aphid complex thus illustrates how ecological divergence can be sustained among many hybridizing populations and how insect host races blend into species by gradual reduction of gene flow. divergent selection ͉ ecological speciation ͉ hybridization ͉ sympatric speciation ͉ phytophagous insects T he beginning of this century has seen the reconciliation of Darwin's view that species gradually emerge by the primary action of natural selection, with the modern evolutionary synthesis defining speciation as the evolution of reproductive isolation (1-4). Adaptations to different habitats and resources may induce reproductive isolation (reviewed in refs. 1, 5, and 6) if morphology or niche selection determines mate choice and if hybrids between ecologically divergent taxa are unfit in the parental environments. Theoretical models and recent empirical studies (reviewed in refs. 7 and 8) have shown that these ecological reproductive barriers may evolve without the geographical separation of populations, an extrinsic barrier to hybridization (gene flow) that was long thought to be a requisite for speciation in animals (2). Divergence in sympatry (i.e., within the same region) implies a more gradual reduction of gene flow that should reflect increasing reproductive isolation and the continuum of speciation from polymorphic populations to good species. Such evolution is not observable in nature at reasonable timescales, but it could be inferred from the multiple stages of sympatric divergence observed within a variety of organisms (9). In phytophagous insects, ''host races'' constitute these intermediate stages of speciation. Host races refer to sympatric populations in partial reproductive isolation that are specialized to different host plants (10-12). Although host race formation can be rapid (12)(13)(14), their transition into full species and the reduction of gene flow during the final stages of speciation have remained difficult to trace. Host races are characterized in very few insect s...

Whole-genome re-sequencing of non-model organisms: lessons from unmapped reads

“…One extreme case is the L. pratensis biotype, which is known to be the most divergent biotype and is considered a cryptic species (Peccoud et al, 2009a). It showed a very specific profile on the heatmap with strong similarity within this biotype (yellow group on Figure 3): a L. pratensis individual shared on average 72% of its unmapped reads with another L. pratensis individual, whereas only 23% were shared with an individual of another biotype.…”

“…Pools of unmapped read sets were used as inputs to obtain sufficient coverage for good quality assemblies. As the individual classification accorded with the biotype composition and because individuals from the same biotype are genetically closer than those from other biotypes (Peccoud et al, 2009a), we pooled unmapped reads that were shared between at least two of the three individuals that belonged to the same biotype. By removing reads uniquely present in a single individual, putatively low coverage sequences were excluded, limiting one potential source of noise to the assembly process.…”

“…This species forms a complex of sympatric populations, or biotypes, each specialized on one or a few legume species (Simon et al, 2003;Via, 1991). Peccoud et al (2009a) showed that these biotypes include at least eight partially reproductively isolated host races and three cryptic species, forming a gradient of specialization and differentiation potentially through ecological speciation. This complex of biotypes started to diverge between 8000 and 16 000 years ago, with a burst of diversification at an estimated 3600-9500 years (Peccoud et al, 2009b).…”

Transitions between phases of genomic differentiation during stick-insect speciation

“…Evidence for divergent selection promoting this process (rather 13 than genome-wide drift) is bolstered if: (1) gene flow is still appreciable, (2) genome-wide 14 differentiation is correlated with environmental differences or traits under divergent selection 15 (i.e., genome-wide 'isolation-by-adaptation', IBA) 11,12 , and (3) genome-wide responses to 16 selection are confirmed with experiments [13][14][15] . Genome-wide differences have been 17 documented in herring 16 , mosquitoes 17 , and apple-maggot flies 10,14 , and genome-wide IBA has 18 been reported in many organisms 11,12 . Notably, theory predicts genomic differentiation can be 19 promoted by polygenic adaptation 3 , epistasis 18 , the coupling of differentiation across loci (as in 20 hybrid zone theory) 19 , and mate choice 20,21 .…”

Evidence for specificity in symbiont-conferred protection against parasitoids

“…Second, we asked whether there are consistent differences in different pea aphid biotypes in their resistance to parasitoid attack. The pea aphid taxon comprises a set of genetically differentiated populations or biotypes which feed on different host plants [39] and which show consistent differences in their symbiont communities [40]. This will help us address whether biotype differentiation is influenced by selection pressures from higher trophic levels in addition to selection for host plant utilization.…”