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Risks of postintroduction evolution in insects introduced to control invasive pests have been discussed for some time, but little is known about responses to selection or genetic architectures of host adaptation and thus about the likelihood or rapidity of evolutionary shifts. We report here results on the response to selection and genetic architecture of parasitism of a suboptimal, low‐preference host species by an aphid parasitoid, Aphelinus rhamni, a candidate for introduction against the soy bean aphid, Aphis glycines. We selected A. rhamni for increased parasitism of Rhopalsiphum padi by rearing the parasitoid on this aphid for three generations. We measured parasitism of R. padi at generations 2 and 3, and at generation 3, we crossed and backcrossed parasitoids from the populations reared on R. padi with those from populations reared on Aphis glycines and compared parasitism of both R. padi and Aphis glycines among F1 and backcross females. Aphelinus rhamni responded rapidly to selection for parasitism of R. padi. Selection for R. padi parasitism reduced parasitism of Aphis glycines, the original host of A. rhamni. However, parasitism of R. padi did not increase from generation 2 to generation 3 of selection, suggesting reduced variance available for selection, which was indeed found. We tested the associations between 184 single nucleotide polymorphisms (SNP) and increased parasitism of R. padi and found 28 SNP loci, some of which were associated with increased and others with decreased parasitism of R. padi. We assembled and annotated the A. rhamni genome, mapped all SNP loci to contigs and tested whether genes on contigs with SNP loci associated with parasitism were enriched for candidate genes or gene functions. We identified 80 genes on these contigs that mapped to 1.2 Mb of the 483 Mb genome of A. rhamni but found little enrichment of candidate genes or gene functions.

Safe, effective biological-control introductions against invasive pests depend on narrowly host-specific natural enemies with the ability to adapt to a changing environment. As part of a project on the genetic architectures of these traits, we assembled and annotated the genomes of two aphid parasitoids, Aphelinus atriplicis and Aphelinus certus. We report here several assemblies of A. atriplicis made with Illumina and PacBio data, which we combined into a meta-assembly. We scaffolded the meta-assembly with markers from a genetic map of hybrids between A. atriplicis and A. certus. We used this genetic-linkage scaffolded (GLS) assembly of A. atriplicis to scaffold a de novo assembly of A. certus. The de novo assemblies of A. atriplicis differed in contiguity, and the meta-assembly of these assemblies was more contiguous than the best de novo assembly. Scaffolding with genetic-linkage data allowed chromosomal-level assembly of the A. atriplicis genome and scaffolding a de novo assembly of A. certus with this GLS assembly, greatly increased the contiguity of the A. certus assembly to the point where it was also at the chromosomal-level. However, completeness of the A. atriplicis assembly, as measured by percent complete, single-copy BUSCO hymenopteran genes, varied little among de novo assemblies and was not increased by meta-assembly or genetic scaffolding. Furthermore, the greater contiguity of the meta-assembly and GLS assembly had little or no effect on the numbers of genes identified, the proportions with homologs or functional annotations. Increased contiguity of the A. certus assembly provided modest improvement in assembly completeness, as measured by percent complete, single-copy BUSCO hymenopteran genes. The total genic sequence increased, and while the number of genes declined, gene length increased, which together suggest greater accuracy of gene models. More contiguous assemblies provide uses other than gene annotation, for example, identifying the genes associated with quantitative trait loci and understanding of chromosomal rearrangements associated with speciation.

We consider the possibility of an extensive invasional meltdown occurring in central North America involving eleven Eurasian species. The scenario begins with the potential co-facilitation between the European earthworm Lumbricus terrestris and European buckthorn, Rhamnus cathartica. Once introduced, European buckthorn has served as the overwintering host for two important invasive crop pests, oat crown rust, Puccinea coronata and the soybean aphid, Aphis glycines. The spread of R. cathartica itself may have been aided by seed dispersal by the European starling, Sturnus vulgaris, and the presence of L. terrestris has likely facilitated the invasion of Bipalium adventitium, an Asian predatory flatworm that specializes on earthworms. Beyond this, the soybean aphid is consumed by a number of introduced species, including the lady beetle Harmonia axyridis, the ground beetle Agonum muelleri and the parasitoid Aphelinus certus. We hypothesize that the presence of soybean aphid increases regional abundances of these species. We discuss both the evidence for this multi-species invasional meltdown scenario and potential implications of meltdown dynamics for invasive species management. The particular management issues that we discuss are: (1) opportunities for managing multiple invasive species simultaneously by targeting facilitator species, and (2) implications of meltdown dynamics for biological control introductions against the soybean aphid.

Leptopilina heterotoma are obligate parasitoid wasps that develop in the body of their Drosophila hosts. During oviposition, female wasps introduce venom into the larval hosts’ body cavity. The venom contains discrete, 300 nm-wide, mixed-strategy extracellular vesicles (MSEVs), until recently referred to as virus-like particles. While the crucial immune suppressive functions of L. heterotoma MSEVs have remained undisputed, their biotic nature and origin still remain controversial. In recent proteomics analyses of L. heterotoma MSEVs, we identified 161 proteins in three classes: conserved eukaryotic proteins, infection and immunity related proteins, and proteins without clear annotation. Here we report 246 additional proteins from the L. heterotoma MSEV proteome. An enrichment analysis of the entire proteome supports vesicular nature of these structures. Sequences for more than 90% of these proteins are present in the whole-body transcriptome. Sequencing and de novo assembly of the 460 Mb-sized L. heterotoma genome revealed 90% of MSEV proteins have coding regions within the genomic scaffolds. Altogether, these results explain the stable association of MSEVs with their wasps, and like other wasp structures, their vertical inheritance. While our results do not rule out a viral origin of MSEVs, they suggest that a similar strategy for co-opting cellular machinery for immune suppression may be shared by other wasps to gain advantage over their hosts. These results are relevant to our understanding of the evolution of figitid and related wasp species.

Parasitic wasps are among the most species‐rich groups on Earth. A major cause of this diversity may be local adaptation to host species. However, little is known about variation in host specificity among populations within parasitoid species. Not only is such knowledge important for understanding host‐driven speciation, but because parasitoids often control pest insects and narrow host ranges are critical for the safety of biological control introductions, understanding variation in specificity and how it arises are crucial applications in evolutionary biology. Here, we report experiments on variation in host specificity among 16 populations of an aphid parasitoid, Aphelinus certus. We addressed several questions about local adaptation: Do parasitoid populations differ in host ranges or in levels of parasitism of aphid species within their host range? Are differences in parasitism among parasitoid populations related to geographical distance, suggesting clinal variation in abundances of aphid species? Or do nearby parasitoid populations differ in host use, as would be expected if differences in aphid abundances, and thus selection, were mosaic? Are differences in parasitism among parasitoid populations related to genetic distances among them? To answer these questions, we measured parasitism of a taxonomically diverse group of aphid species in laboratory experiments. Host range was the same for all the parasitoid populations, but levels of parasitism varied among aphid species, suggesting adaptation to locally abundant aphids. Differences in host specificity did not correlate with geographical distances among parasitoid populations, suggesting that local adaption is mosaic rather than clinal, with a spatial scale of less than 50 kilometers. We sequenced and assembled the genome of A. certus, made reduced‐representation libraries for each population, analyzed for single nucleotide polymorphisms, and used these polymorphisms to estimate genetic differentiation among populations. Differences in host specificity correlated with genetic distances among the parasitoid populations.

▪ Abstract  In evolutionary ecology, risk-spreading (i.e. bet-hedging) is the idea that unpredictably variable environments favor genotypes with lower variance in fitness at the cost of lower arithmetic mean fitness. Variance in fitness can be reduced by physiology or behavior that spreads risk of encountering an unfavorable environment over time or space. Such risk-spreading can be achieved by a single phenotype that avoids risks (conservative risk-spreading) or by phenotypic variation expressed by a single genotype (diversified risk-spreading). Across these categories, three types of risk-spreading can be usefully distinguished: temporal, metapopulation, and within-generation. Theory suggests that temporal and metapopulation risk-spreading may work under a broad range of population sizes, but within-generation risk-spreading appears to work only when populations are small. Although genetic polymorphisms have sometimes been treated as risk-spreading, the underlying mechanisms are different, and they often require different conditions for their evolution and thus are better treated separately. I review the types of evidence that could be used to test for risk-spreading and discuss evidence for risk-spreading in facultative diapause, migration polyphenism, spatial distribution of oviposition, egg size, and other miscellaneous traits. Although risk-spreading theory is voluminous and well developed in some ways, rarely has it been used to generate detailed, testable hypotheses about the evolution of risk-spreading. Furthermore, although there is evidence for risk-spreading, particularly in facultative diapause, I have been unable to find any definitive tests with unequivocal results showing that risk-spreading has been a major factor in the evolution of insect behaviors or life histories. To advance our understanding of risk-spreading in the wild, we need (a) explicit empirical models that predict levels of diversifying risk-spreading for several insect populations in several environments that vary in uncertainty, and (b) tests of these models using measurements of phenotypes and their fitnesses over several generations in each environment.

High-throughput sequencing (HTS) of reduced representation genomic libraries has ushered in an era of genotyping-by-sequencing (GBS), where genome-wide genotype data can be obtained for nearly any species. However, there remains a need for imputation-free GBS methods for genotyping large samples taken from heterogeneous populations of heterozygous individuals. This requires that a number of issues encountered with GBS be considered, including the sequencing of nonoverlapping sets of loci across multiple GBS libraries, a common missing data problem that results in low call rates for markers per individual, and a tendency for applicability only in inbred line samples with sufficient linkage disequilibrium for accurate imputation. We addressed these issues while developing and validating a new, comprehensive platform for GBS. This study supports the notion that GBS can be tailored to particular aims, and using Zea mays our results indicate that large samples of unknown pedigree can be genotyped to obtain complete and accurate GBS data. Optimizing size selection to sequence a high proportion of shared loci among individuals in different libraries and using simple in silico filters, a GBS procedure was established that produces high call rates per marker (>85%) with accuracy exceeding 99.4%. Furthermore, by capitalizing on the sequence-read structure of GBS data (stacks of reads), a new tool for resolving local haplotypes and scoring phased genotypes was developed, a feature that is not available in many GBS pipelines. Using local haplotypes reduces the marker dimensionality of the genotype matrix while increasing the informativeness of the data. Phased GBS in maize also revealed the existence of reproducibly inaccurate (apparent accuracy) genotypes that were due to divergent copy number variants (CNVs) unobservable in the underlying single nucleotide polymorphism (SNP) data.

The pores and associated glands on male antennae in species of Hymenoptera are involved in mate recognition and are diverse and widespread among taxa. However, nothing has been published about these structures in species of Aphelinus (Chalcidoidea: Aphelinidae), a genus of parasitoid wasps with a long history in biological control. Images from scanning electron microscopy (SEM) and transmission electron microscopy (TEM) of Aphelinus varipes revealed pores on the ventral side of the male scape that were connected to glands. A survey of the scapes of male antennae in 16 species in six species complexes of Aphelinus , as well as two outgroup species, Aphytis melinus and Centrodora sp., showed that pores were present in all except Centrodora sp. The pores varied in several characters: the shape of the structures that carried them, pore size, elevation of the cuticle surrounding the structures, the extent of a carina delimiting the area around the structures, and the number and position of pores. The shape of the pore-bearing structures, the elevation of cuticle around these structures, and the extent of the carina around them map well onto a molecular phylogeny of these Aphelinus species. Combinations of pore characters are diagnostic of species complexes, and in some cases, species of Aphelinus .

Aphelinus (Hymenoptera: Aphelinidae) is a genus of parasitoid wasps that has a long history of use in biological control programs against aphids. Past research shows that species delimitation within Aphelinus is greatly complicated by lack of comprehensive literature and the existence of cryptic species complexes. One of these complexes is the Aphelinus asychis species group. Through the development of a morphological character set, a revision of the Aphelinus asychis species group was conducted. Two new species, Aphelinus sinensis sp. n. , and Aphelinus kazakhstanensis sp. n. , are described, and the two existing valid species within the asychis group, Aphelinus asychis and Aphelinus semiflavus are redescribed and lectotypes are designated for Aphelinus semiflavus and Aphelinus brevipennis (a junior synonym of Aphelinus semiflavus ). We also provide a key for identifying species in the asychis group.

Broad-spectrum insecticides are the main control measure of the invasive and economically damaging soybean aphid ( Aphis glycines ) in North America, although biological control by resident natural enemies can also greatly diminish population levels. One such natural enemy is the accidentally introduced Eurasian parasitoid Aphelinus certus (Hymenoptera: Aphelinidae), though its impact appears to be limited by low rates of parasitism early in the growing season. We tested the hypothesis that A. certus might experience high overwintering mortality. In the laboratory, we used thermocouple thermometry to measure the supercooling points of diapausing parasitoids and assessed parasitoid survival after exposure to ecologically relevant durations of low temperature. We found A. certus to be freeze-intolerant with a median supercooling point of −28°C. When exposed to temperatures of 0°C for up to 7 months, adults emerged only after exposures of at least 60 days and survival decreased with durations beyond 150 days. We also conducted in-field studies at sites from northern Minnesota to southern Iowa to determine if diapausing A. certus could overwinter above and below the snowpack. Survival was negatively correlated with increasing latitude and was greater for parasitoids placed on the ground than 1 meter off the ground, likely due to the warmer and stabler temperatures of the subnivean microclimate. Our results suggest that A. certus is capable of overwintering in the region inhabited by soybean aphid but may experience substantial mortality even under ideal conditions. Climate change is predicted to bring warmer, drier winters to the North American Midwest, with decreased depth and duration of snow cover, which may further reduce overwintering survival.