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Title: Evolutionary genetics of host shifts in herbivorous insects: insights from the age of genomics: The genomics of insect host shifts
Author(s) / Creator(s):
Publisher / Repository:
Date Published:
Journal Name:
Annals of the New York Academy of Sciences
Page Range / eLocation ID:
186 to 212
Medium: X
Sponsoring Org:
National Science Foundation
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  1. Studies assessing the predictability of evolution typically focus on short-term adaptation within populations or the repeatability of change among lineages. A missing consideration in speciation research is to determine whether natural selection predictably transforms standing genetic variation within populations into differences between species. Here, we test whether and how host-related selection on diapause timing associates with genome-wide differentiation during ecological speciation by comparing ancestral hawthorn and newly formed apple-infesting host races of Rhagoletis pomonella to their sibling species Rhagoletis mendax that attacks blueberries. The associations of 57 857 single nucleotide polymorphisms in a diapause genome-wide-association study (GWAS) on the hawthorn race strongly predicted the direction and magnitude of genomic divergence among the three fly populations at a field site in Fennville, MI, USA. The apple race and R. mendax show parallel changes in the frequencies of putative inversions on three chromosomes associated with the earlier fruiting times of apples and blueberries compared to hawthorns. A diapause GWAS on R. mendax revealed compensatory changes throughout the genome accounting for the earlier eclosion of blueberry, but not apple flies. Thus, a degree of predictability, although not complete, exists in the genomics of diapause across the ecological speciation continuum in Rhagoletis . The generality of this result is placed in the context of other similar systems. This article is part of the theme issue ‘Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'. 
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  2. Genes that affect adaptive traits have been identified, but our knowledge of the genetic basis of adaptation in a more general sense (across multiple traits) remains limited. We combined population-genomic analyses of evolve-and-resequence experiments, genome-wide association mapping of performance traits, and analyses of gene expression to fill this knowledge gap and shed light on the genomics of adaptation to a marginal host (lentil) by the seed beetle Callosobruchus maculatus. Using population-genomic approaches, we detected modest parallelism in allele frequency change across replicate lines during adaptation to lentil. Mapping populations derived from each lentil-adapted line revealed a polygenic basis for two host-specific performance traits (weight and development time), which had low to modest heritabilities. We found less evidence of parallelism in genotype-phenotype associations across these lines than in allele frequency changes during the experiments. Differential gene expression caused by differences in recent evolutionary history exceeded that caused by immediate rearing host. Together, the three genomic datasets suggest that genes affecting traits other than weight and development time are likely to be the main causes of parallel evolution and that detoxification genes (especially cytochrome P450s and beta-glucosidase) could be especially important for colonization of lentil by C. maculatus. 
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  3. Summary

    Insects in the Auchenorrhyncha (Hemiptera: Suborder) established nutritional symbioses with bacteria approximately 300 million years ago (MYA). The suborder split early during its diversification (~ 250 MYA) into the Fulgoroidea (planthoppers) and Cicadomorpha (leafhoppers and cicadas). The two lineages share some symbionts, includingSulciaand possibly aBetaproteobacteriathat collaboratively provide their hosts with 10 essential amino acids (EAA). Some hosts harbour three bacteria, as is common among planthoppers. However, genomic studies are currently restricted to the dual‐bacterial symbioses found in Cicadomorpha, leaving the origins and functions of these more complex symbioses unclear. To address these questions, we sequenced the genomes and performed phylogenomic analyses of ‘CandidatusSulcia muelleri’ (Bacteroidetes), ‘Ca. Vidania fulgoroideae’ (Betaproteobacteria) and ‘Ca. Purcelliella pentastirinorum’ (Gammaproteobacteria) from a planthopper (Cixiidae:Oliarus). In contrast to the Cicadomorpha, nutritional synthesis responsibilities are rearranged between the cixiid symbionts. AlthoughSulciahas a highly conserved genome across the Auchenorrhyncha, in the cixiids it is greatly reduced and provides only three EAAs.Vidaniacontributes the remaining seven EAAs. Phylogenomic results suggest that it represents an ancient symbiont lineage paired withSulciathroughout the Auchenorrhyncha. Finally,Purcelliellawas recently acquired from plant‐insect associated bacteria (PantoeaErwinia) to provide B vitamins and metabolic support to its degenerate partners.

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