Hybridisation has shaped a recent radiation of grass-feeding aphids

Mathers, Thomas C., Wouters, Roland H. M., Mugford, Sam T., Biello, Roberto, van Oosterhout, Cock ORCID: https://orcid.org/0000-0002-5653-738X and Hogenhout, Saskia A. (2023) Hybridisation has shaped a recent radiation of grass-feeding aphids. BMC Biology, 21. ISSN 1741-7007

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Background: Aphids are common crop pests. These insects reproduce by facultative parthenogenesis involving several rounds of clonal reproduction interspersed with an occasional sexual cycle. Furthermore, clonal aphids give birth to live young that are already pregnant. These qualities enable rapid population growth and have facilitated the colonisation of crops globally. In several cases, so-called “super clones” have come to dominate agricultural systems. However, the extent to which the sexual stage of the aphid life cycle has shaped global pest populations has remained unclear, as have the origins of successful lineages. Here, we used chromosome-scale genome assemblies to disentangle the evolution of two global pests of cereals—the English (Sitobion avenae) and Indian (Sitobion miscanthi) grain aphids.   Results: Genome-wide divergence between S. avenae and S. miscanthi is low. Moreover, comparison of haplotype-resolved assemblies revealed that the S. miscanthi isolate used for genome sequencing is likely a hybrid, with one of its diploid genome copies closely related to S. avenae (~ 0.5% divergence) and the other substantially more divergent (> 1%). Population genomics analyses of UK and China grain aphids showed that S. avenae and S. miscanthi are part of a cryptic species complex with many highly differentiated lineages that predate the origins of agriculture. The complex consists of hybrid lineages that display a tangled history of hybridisation and genetic introgression.   Conclusions: Our analyses reveal that hybridisation has substantially contributed to grain aphid diversity, and hence, to the evolutionary potential of this important pest species. Furthermore, we propose that aphids are particularly well placed to exploit hybridisation events via the rapid propagation of live-born “frozen hybrids” via asexual reproduction, increasing the likelihood of hybrid lineage formation.

Item Type: Article
Additional Information: Funding information: The described work was supported by a Biotechnology and Biological Sciences Research Council (BBSRC) grant (BB/R009481/1) and a CEPAMS grant (17.03.2) awarded to S.A.H. and a BBSRC Future Leader Fellowship (BB/R01227X/1) awarded to T.C.M.. R.H.M.W. was funded from the BBSRC Norwich Research Park Biosciences Doctoral Training Partnership Award (BB/M011216/1). Additional support was provided by the BBSRC Institute Strategy Programs (BBS/E/J/000PR9797 and BBS/E/J/000PR9798) awarded to the John Innes Centre. The JIC is grant-aided by the John Innes Foundation.
Uncontrolled Keywords: comparative genomics,genome assembly,insect crop pest,introgression,metopolophium dirhodum,population genomics,sitobion avenae,sitobion miscanthi,biotechnology,structural biology,ecology, evolution, behavior and systematics,physiology,biochemistry, genetics and molecular biology(all),agricultural and biological sciences(all),plant science,developmental biology,cell biology ,/dk/atira/pure/subjectarea/asjc/1300/1305
Faculty \ School: Faculty of Science > School of Biological Sciences
Faculty of Science > School of Environmental Sciences
UEA Research Groups: Faculty of Science > Research Centres > Centre for Ecology, Evolution and Conservation
Related URLs:
Depositing User: LivePure Connector
Date Deposited: 21 Jul 2023 13:30
Last Modified: 09 Mar 2024 12:31
URI: https://ueaeprints.uea.ac.uk/id/eprint/92650
DOI: 10.1186/s12915-023-01649-4


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