Molecular and behavioural evidence for gene flow between host races of the larch budmoth Zeiraphera diniana

Larch and pine associated populations of Zeiraphera diniana (Lepidoptera: Tortricidae) differ in a number of heritable traits, but pheromone-mediated cross-attraction occurs between them in the wild. Using a quartet mate choice design (one male and one female of each type per cage) we estimate that, following cross-attraction by pheromones, the subsequent probability of hybridization is approximately 28%. We also examined molecular data, and were unable to distinguish between the races on the basis of 695bp of mitochondrial COI, tRNA-leucine, and COII gene sequence. Both results support earlier field studies suggesting that larch- and pine-feeding populations are host races that hybridize at an appreciable level in the wild. The shared mitochondrial haplotypes we observed are also consistent with ongoing and successful gene flow between the two host races

Evidence for suppression of immunity as a driver for genomic introgressions and host range expansion in races of Albugo candida, a generalist parasite

How generalist parasites with wide host ranges can evolve is a central question in parasite evolution. Albugo candida is an obligate biotrophic parasite that consists of many physiological races that each specialize on distinct Brassicaceae host species. By analyzing genome sequence assemblies of five isolates, we show they represent three races that are genetically diverged by ∼1%. Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races. Sequential infection experiments show that infection by adapted races enables subsequent infection of hosts by normally non-infecting races. This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts. We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin’s finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment

Targeted re-sequencing confirms the importance of chemosensory genes in aphid host race differentiation.

Host-associated races of phytophagous insects provide a model for understanding how adaptation to a new environment can lead to reproductive isolation and speciation, ultimately enabling us to connect barriers to gene flow to adaptive causes of divergence. The pea aphid (Acyrthosiphon pisum) comprises host-races specialising on legume species, and provides a unique system for examining the early stages of diversification along a gradient of genetic and associated adaptive divergence. As host-choice produces assortative mating, understanding the underlying mechanisms of choice will contribute directly to understanding of speciation. As host-choice in the pea aphid is likely mediated by smell and taste, we use capture sequencing and SNP genotyping to test for the role of chemosensory genes in the divergence between eight host-plant species across the continuum of differentiation and sampled at multiple locations across western Europe. We show high differentiation of chemosensory loci relative to control loci in a broad set of pea aphid races and localities, using a model-free approach based on Principal Component analysis. Olfactory and gustatory receptors form the majority of highly differentiated genes, and include loci that were already identified as outliers in a previous study focusing on the three most closely related host races. Consistent indications that chemosensory genes may be good candidates for local adaptation and barriers to gene flow in the pea aphid open the way to further investigations aiming to understand their impact on gene flow, and to determine their precise functions in response to host plant metabolites. This article is protected by copyright. All rights reserved

The chemical signatures underlying host plant discrimination by aphids

The diversity of phytophagous insects is largely attributable to speciation involving shifts between host plants. These shifts are mediated by the close interaction between insects and plant metabolites. However, there has been limited progress in understanding the chemical signatures that underlie host preferences. We use the pea aphid (Acyrthosiphon pisum) to address this problem. Host-associated races of pea aphid discriminate between plant species in race-specific ways. We combined metabolomic profiling of multiple plant species with behavioural tests on two A. pisum races, to identify metabolites that explain variation in either acceptance or discrimination. Candidate compounds were identified using tandem mass spectrometry. Our results reveal a small number of compounds that explain a large proportion of variation in the differential acceptability of plants to A. pisum races. Two of these were identified as L-phenylalanine and L-tyrosine but it may be that metabolically-related compounds directly influence insect behaviour. The compounds implicated in differential acceptability were not related to the set correlated with general acceptability of plants to aphids, regardless of host race. Small changes in response to common metabolites may underlie host shifts. This study opens new opportunities for understanding the mechanistic basis of host discrimination and host shifts in insects

Genetic Structure in the Seabuckthorn Carpenter Moth (Holcocerus hippophaecolus) in China: The Role of Outbreak Events, Geographical and Host Factors

Understanding factors responsible for structuring genetic diversity is of fundamental importance in evolutionary biology. The seabuckthorn carpenter moth (Holcocerus hippophaecolus Hua) is a native species throughout the north of China and is considered the main threat to seabuckthorn, Hippophae rhamnoides L. We assessed the influence of outbreaks, environmental factors and host species in shaping the genetic variation and structure of H. hippophaecolus by using Amplified Fragment Length Polymorphism (AFLP) markers. We rejected the hypothesis that outbreak-associated genetic divergence exist, as evidenced by genetic clusters containing a combination of populations from historical outbreak areas, as well as non-outbreak areas. Although a small number of markers (4 of 933 loci) were identified as candidates under selection in response to population densities. H. hippophaecolus also did not follow an isolation-by-distance pattern. We rejected the hypothesis that outbreak and drought events were driving the genetic structure of H. hippophaecolus. Rather, the genetic structure appears to be influenced by various confounding bio-geographical factors. There were detectable genetic differences between H. hippophaecolus occupying different host trees from within the same geographic location. Host-associated genetic divergence should be confirmed by further investigation

Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects

The degree of phenotypic divergence and reproductive isolation between taxon pairs can vary quantitatively, and often increases as evolutionary divergence proceeds through various stages, from polymorphism to population differentiation, ecotype and race formation, speciation, and post-speciational divergence. Although divergent natural selection promotes divergence, it does not always result in strong differentiation. For example, divergent selection can fail to complete speciation, and distinct species pairs sometimes collapse (‘speciation in reverse’). Widely-discussed explanations for this variability concern genetic architecture, and the geographic arrangement of populations. A less-explored possibility is that the degree of phenotypic and reproductive divergence between taxon pairs is positively related to the number of ecological niche dimensions (i.e., traits) subject to divergent selection. Some data supporting this idea stem from laboratory experimental evolution studies using Drosophila, but tests from nature are lacking. Here we report results from manipulative field experiments in natural populations of herbivorous Timema stick insects that are consistent with this ‘niche dimensionality’ hypothesis. In such insects, divergent selection between host plants might occur for cryptic colouration (camouflage to evade visual predation), physiology (to detoxify plant chemicals), or both of these niche dimensions. We show that divergent selection on the single niche dimension of cryptic colouration can result in ecotype formation and intermediate levels of phenotypic and reproductive divergence between populations feeding on different hosts. However, greater divergence between a species pair involved divergent selection on both niche dimensions. Although further replication of the trends reported here is required, the results suggest that dimensionality of selection may complement genetic and geographic explanations for the degree of diversification in nature

Partitioning of herbivore hosts across time and food plants promotes diversification in the <i>Megastigmus dorsalis</i> oak gall parasitoid complex

Communities of insect herbivores and their natural enemies are rich and ecologically crucial components of terrestrial biodiversity. Understanding the processes that promote their origin and maintenance is thus of considerable interest. One major proposed mechanism is ecological speciation through host-associated differentiation (HAD), the divergence of a polyphagous species first into ecological host races and eventually into more specialized daughter species. The rich chalcid parasitoid communities attacking cynipid oak gall wasp hosts are structured by multiple host traits, including food plant taxon, host gall phenology, and gall structure. Here, we ask whether the same traits structure genetic diversity within supposedly generalist parasitoid morphospecies. We use mitochondrial DNA sequences and microsatellite genotypes to quantify HAD for Megastigmus (Bootanomyia) dorsalis, a complex of two apparently generalist cryptic parasitoid species attacking oak galls. Ancient Balkan refugial populations showed phenological separation between the cryptic species, one primarily attacking spring galls, and the other mainly attacking autumn galls. The spring species also contained host races specializing on galls developing on different host- plant lineages (sections Cerris vs. Quercus) within the oak genus Quercus. These results indicate more significant host-associated structuring within oak gall parasitoid communities than previously thought and support ecological theory predicting the evolution of specialist lineages within generalist parasitoids. In contrast, UK populations of the autumn cryptic species associated with both native and recently invading oak gall wasps showed no evidence of population differentiation, implying rapid recruitment of native parasitoid populations onto invading hosts, and hence potential for natural biological control. This is of significance given recent rapid range expansion of the economically damaging chestnut gall wasp, Dryocosmus kuriphilus, in Europe

Dynamics of copy number variation in host races of the pea aphid.

Copy number variation (CNV) makes a major contribution to overall genetic variation and is suspected to play an important role in adaptation. However, aside from a few model species, the extent of CNV in natural populations has seldom been investigated. Here, we report on CNV in the pea aphid Acyrthosiphon pisum, a powerful system for studying the genetic architecture of host-plant adaptation and speciation thanks to multiple host races forming a continuum of genetic divergence. Recent studies have highlighted the potential importance of chemosensory genes, including the gustatory and olfactory receptor gene families (Gr and Or, respectively), in the process of host race formation. We used targeted resequencing to achieve a very high depth of coverage, and thereby revealed the extent of CNV of 434 genes, including 150 chemosensory genes, in 104 individuals distributed across eight host races of the pea aphid. We found that CNV was widespread in our global sample, with a significantly higher occurrence in multigene families, especially in Ors. We also observed a decrease in the gene probability of being completely duplicated or deleted (CDD) with increase in coding sequence length. Genes with CDD variants were usually more polymorphic for copy number, especially in the P450 gene family where toxin resistance may be related to gene dosage. We found that Gr were overrepresented among genes discriminating host races, as were CDD genes and pseudogenes. Our observations shed new light on CNV dynamics and are consistent with CNV playing a role in both local adaptation and speciation