Cranston, Peter

Simonsen, Thomas J.

Weirauch, Christiane

Winterton, Shaun L.

The Australian National University

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/341678669New ways for old specimens - museomics is transforming the field ofsystematic entomologyArticle · May 2020CITATIONS0READS3024 authors, including:Some of the authors of this publication are also working on these related projects:see title View projectTaxonomy of Osmylidae View projectChristiane WeirauchUniversity of California, Riverside211 PUBLICATIONS   1,775 CITATIONS   SEE PROFILEPeter CranstonAustralian National University150 PUBLICATIONS   4,898 CITATIONS   SEE PROFILEShaun L WintertonCalifornia Department of Food and Agriculture260 PUBLICATIONS   2,631 CITATIONS   SEE PROFILEAll content following this page was uploaded by Shaun L Winterton on 29 May 2020.The user has requested enhancement of the downloaded file.22 Antenna 2020: 44 (1)work on almost every insect-related topic imaginable. Withthis in mind, the RES trustees have agreed to fund andoversee an ambitious project in collaboration with the wholeRES membership that will culminate in a “state ofentomology” paper to outline the major challenges ahead inentomology. These will then be unpacked to reveal specificresearch questions related to each wider challenge. Dr LynnDicks FRES (University of Cambridge) will be the leadresearcher on a survey of the RES membership. The aim isto use the wealth of experience and knowledge of the Societyto inform policymakers, funding bodies and the public aboutthe challenges ahead and how entomology might offersolutions. To achieve this, Dr Dicks’ project will run fromJanuary to September 2020 and every Member, Fellow andHonorary Fellow will receive a survey in order to take partin this exciting initiative. The information gathered will thenbe synthesised and summarised using workshops and globalexperts to compile a report.I sincerely hope that you will choose to participate andhelp to create a valuable “state of entomology” paper thatwill act as a manifesto for the future of global insect science.You should expect to hear from Dr Dicks in the near future.Please add your experience to the project.Journals and LibraryNatural history collections have preserved and housednatural objects since the “cabinets of curiosities” of theRenaissance period. Still, only a minute proportion of theirvast holdings is on display in the public galleries of thesenatural history museums. The remaining billions of biologicalspecimens worldwide are archived behind the scenes, in whatmight be envisioned as dusty and dark vaults reluctant toreveal their treasures. Until the second half of the 20thcentury, these collections have almost exclusively served asresource for the cataloguing and classifying of past andpresent biodiversity including the discovery anddocumentation of taxa so far unknown to science. Thisstarted to change before the turn of the millennium, whenscientists launched the first large initiatives to “unlock thevault” and bring the vast biodiversity data harboured inbiological collections out into the open by creating digitalrecords of the metadata associated with a specimen (locality,date, collector, host plant, etc.), imaging of specimens, and bymaking these data freely available online. This biodiversityinformatics revolution was spearheaded initially by museumscientists and curators focussed on vertebrates and plants,because of the larger size, greater public interest, moremanageable number of specimens, and the 2D quality ofherbarium specimens that facilitate workflows. Althoughmore challenging because of the enormous number ofspecimens, comparatively small size, diversity of preservationtechniques, and position of metadata on a label underneaththe specimen, a growing number of specimens inentomological collections worldwide have been, or arecurrently being, digitized1,2. By documenting past and presentand predicting future species distribution ranges, thesemuseum-derived datasets have enabled research on areasincluding biodiversity change in relation to climate change,biological invasions, and arthropod vectors of public andveterinary health concerns, impacting fields far beyondsystematic entomology3,4. Fig. 1. Samantha Smith (Weirauch lab, UC Riverside) collectingemesine assassin bugs for phylogenomic projects on Barro ColoradoIsland, Panama.New ways for old specimens –museomics is transforming the field ofsystematic entomologyChristiane Weirauch, Peter S. Cranston, Thomas J. Simonsen and Shaun L. WintertonEditors of Systematic EntomologyWe are now at a point where an on-going revolution inDNA-sequencing techniques and bioinformaticsmethodology allows us to unlock this vault of treasures evenfurther5. Starting in the mid-2000s, advances in sequencingtechnology have launched research that is now referred to as“museomics”, a legacy approach to genetic sequencing ofspecimens from museum collections. In contrast to moreAntenna 44(1).qxp_Layout 1  01/04/2020  14:36  Page 22Antenna 2020: 44 (1) 23traditional molecular systematics projects that requiredtargeted field-work (Fig. 1) and careful preservation of tissuesto ensure that DNA remains largely intact, these newapproaches take advantage of the billions of specimens thatare already deposited in natural history collections (Fig. 2).Using genetic material and data from specimens in naturalhistory collections, scientists can now trace evolutionaryorigins, model past and future spread of pests and diseases,offer insights into the evolution of insecticide resistance, andrevolutionize our understanding of human evolution usingancient DNA. Similar to the biodiversity informatics revolution,museomics was spearheaded initially by the vertebrate andbotanical communities, but despite the unique set ofchallenges when applied to small, dry biological specimens,insect scientists have made great strides towards embracingand advancing this field 6–8. Studies range from targetingrelatively few genes to entire mitochondrial and/or nucleargenomes. Entomologists have explored the feasibility ofextracting and amplifying DNA from pinned insectspecimens with fragmented and degraded DNA andsubsequent Sanger sequencing for more than two decades9.However, only the use of next-generation sequencing (NGS)protocols that has increased substantially during recent yearshas started to make museomics in the entomological field acost-effective and more widely used alternative to traditionalapproaches. This is largely due to the fact that NGS protocolsinvolve steps that “shear” or fragment intact DNA, so usingalready fragmented DNA from pinned insect specimensshould not pose a problem - at least theoretically. In the realworld, entomological museomics offers great opportunities,but also significant challenges, in particular for pinned, drymuseum specimens that represent the bulk of entomologicalcollections. Due to centuries of field expeditions to all corners of theworld, natural history collections are the mostcomprehensive and accessible representation of biodiversity,offering a tremendous opportunity for scientific discovery.They also house rare species that even targeted expeditionsfrequently fail to find again; these are often represented onlyby the original type specimens. Another great benefit of usingmuseum specimens for genetic research is that generationsof taxonomists may have worked on a given collection andthe proportion of specimens authoritatively identified tospecies level is consequently high. Given that NGSapproaches have recovered sequence data for insectspecimens that were collected more than a century ago,museomics also has the potential to uncover historicalsignatures in genetic sequences, allowing, e.g., an improvedunderstanding of the evolution of insecticide resistance10 andsimilar phenomena such as cryptic (genomic) changeswithin, and between, populations due to well-documentedenvironmental and anthropogenic changes. Generating andmaking publicly available genetic resources is also a keyelement of the Nagoya Protocol on Access to GeneticResources, a supplementary agreement to the Convention onBiological Diversity. Furthermore, in the face of the currentbiodiversity extinction crisis, museum specimens includingbulk samples from large survey and passive trapping projectsmay be the only specimens remaining after the site surveyedis no longer intact. Museomics may thus be the only way toacquire unique genomic insights into the biological,evolutionary and biogeographical importance of now extinctpopulations.Despite these overwhelming benefits, there are stillchallenges to applying museomic approaches to insectspecimens. The number of insect species, both known toscience and remaining undescribed, is staggering and thenumber of insect specimens in collections is overwhelming(300 million in North American collections alone2); theavailability of genome-scale datasets for all, or even just themajority of, insect species is therefore a distant dream. Inaddition, many insects are small and the amount of DNAthat can be retrieved from a single specimen may be too littlefor reliable sequencing without destruction of the entirespecimen. Depending on collecting methods andpreservation conditions, pinned insect specimens can beheavily degraded and even overgrown by fungi, posingadditional challenges to both the wet lab protocols andbioinformatics procedures required to sort useful sequencedata from potential contaminants. Additionally, primarytypes are the only known specimens for many species,making the advancement of protocols for largely non-destructive sampling imperative in like manner as currentlyemployed for procedures such as genitalic dissections. Although NGS approaches are now cost-effectivecompared to Sanger-sequencing projects, sampling of a largenumber of individuals for relatively low-profile projects suchas genus-level taxonomic revisions will benefit from furtherrefining protocols for maximal effectiveness. On-goingresearch is further adapting and optimizing NGS methodsfor pinned museum specimens in an attempt to make themaffordable and widely used11,12. The challenge for museomicswill be how to integrate with the rapidly growing field ofenvironmental DNA that reveals almost inconceivablediversity in terrestrial and especially freshwater aquaticsystems, with much deriving from insects13. While NGSbarcoding allows rapid and low-cost association of insect lifestages14 allowing identifications against well-populated‘libraries’ of organisms, the data produced in such studiesalready seem likely to overwhelm even the most dedicatedmuseomic practitioners. Yet, without such connections withhistoric named specimens, we can ask what value suchmetagenomic revelation of diversity can have in a world ofbiodiversity losses.A conclusion might seem to be that field expeditions andthe collection of  large-scale specimens are things of the past.This is, however, far from the truth. Not only is field-worknecessary to study and document the biology, ecology andbehaviour that museomics may allow us to put into anFig. 2. Madison Hernandez (Weirauch lab, UC Riverside) preparingassassin bug museum specimens for next-generation sequencing.Antenna 44(1).qxp_Layout 1  01/04/2020  14:36  Page 2324 Antenna 2020: 44 (1)evolutionary context, but also continuous collecting activitiesaimed at building collections for the future are essential todocument and explore both spatial and temporal crypticchanges in molecular diversity – changes that are oftenpreceding more obvious phenological, phenotypic orecological changes. In fact, this makes collecting activitieseven more important in the current age of acceleratingbiodiversity changes. Indeed, museomics simply provides anopportunity to exploit the vast wealth of legacy geneticinformation already available in present collections, to thenuse this data source to strategize future research efforts,including field-work. We argue that any decrease in collectingactivities (among both professional and amateurs), or fundingfor collecting and collection maintenance, threatens todeprive future researchers of the opportunity to study andpublish research on our biodiversity in the Society’s journalsin the same way that we have benefited from the collectingactivities of past generations.References1.    Blagoderov V, Kitching IJ, Livermore L, Simonsen TJ, Smith VS. No specimen left behind: Industrial scale digitization of natural history collections.Zookeys. 2012; 209: 133-146. doi:10.3897/zookeys.209.31782.    Cobb NS, Gall LF, Zaspel JM, Dowdy NJ, McCabe LM, Kawahara AY. Assessment of North American arthropod collections: prospects andchallenges for addressing biodiversity research. PeerJ. 2019; 7: e8086. doi:10.7717/peerj.80863.    Baird RC. Leveraging the fullest potential of scientific collections through digitisation. Biodivers. Informatics. 2010; 7(2). doi:10.17161/bi.v7i2.39874.    Zeilinger AR, Rapacciuolo G, Turek D, Oboyski PT, Almeida RPP, Roderick GK. Museum specimen data reveal emergence of a plant disease maybe linked to increases in the insect vector population. Ecol. Appl. 2017; 27(6): 1827-1837. doi:10.1002/eap.15695.    Short AEZ, Dikow T, Moreau CS. Entomological Collections in the age of big data. Annu. Rev. Entomol. 2018; 63(1): 513-530. doi:10.1146/annurev-ento-031616-0355366.    Timmermans MJTN, Viberg C, Martin G, Hopkins K, Vogler AP. Rapid assembly of taxonomically validated mitochondrial genomes from historicalinsect collections. Biol. J. Linn. Soc. 2016; 117(1): 83-95. doi:10.1111/bij.125527.    Kanda K, Pflug JM, Sproul JS, Dasenko MA, Maddison DR. Successful recovery of nuclear protein-coding genes from small insects in museumsusing Illumina sequencing. PLoS One. 2015; 10(12). doi:10.1371/journal.pone.01439298.    Blaimer BB, Lloyd MW, Guillory WX, Brady SG. Sequence capture and phylogenetic utility of genomic ultraconserved elements obtained frompinned insect specimens. O’Grady P, ed. PLoS One. 2016; 11(8): e0161531. doi:10.1371/journal.pone.01615319.    Dillon N, Austin AD, Bartowsky E. Comparison of preservation techniques for DNA extraction from hymenopterous insects. Insect. Mol. Biol.1996; 5(1): 21-24. doi:10.1111/j.1365-2583.1996.tb00036.x10.  Hartley CJ, Newcomb RD, Russell RJ, et al. Amplification of DNA from preserved specimens shows blowflies were preadapted for the rapidevolution of insecticide resistance. Proc. Nat.l Acad. Sci. USA. 2006; 103(23): 8757-8762. doi:10.1073/pnas.050959010311.  Knyshov A, Hoey-Chamberlain R, Weirauch C. Hybrid enrichment of poorly preserved museum specimens refines homology hypotheses in agroup of minute litter bugs (Hemiptera: Dipsocoromorpha: Schizopteridae). Syst. Entomol. June 2019: syen.12368. doi:10.1111/syen.1236812.  Sproul JS, Maddison DR. Sequencing historical specimens: successful preparation of small specimens with low amounts of degraded DNA. Mol.Ecol. Resour. 2017; 17(6): 1183-1201. doi:10.1111/1755-0998.1266013.  Baloglu B, Clews E, & Meier R. NGS barcoding reveals high resistance of a hyperdiverse chironomid (Diptera) swamp fauna against invasion fromadjacent freshwater reservoirs.  Front. Zool. 2018; 15(1), 31.14.  Yeo D,  Puniamoorthy J,  Ngiam RWJ,  Meier R. Towards holomorphology in entomology: rapid and cost-effective adult–larva matching usingNGS barcodes. Syst. Entomol. 2018; 43(4), 678-691.New publication announcementHandbooks for the Identification of British InsectsVol 2. Part 8Aphids – Anoeciinae, Lachninae, Eriosomatinae, Phloeomyzinae, Thelaxinae,Hormaphidinae, MindarinaeBy Roger L. Blackman, Robert D. Dransfield and Robert BrightwellThis is the fourth Royal Entomological Society handbook on aphids, and completes thecoverage of the British species. It covers seven subfamilies, represented in Britain by 105species in 35 genera. They encompass a great diversity of life-styles, ranging from theEulachnini with Cinara and other major pests of conifers, to the Eriosomatini andPemphigini, which induce galls on elms and poplars and then migrate to colonise the rootsof various herbaceous plants. For each subfamily there are keys for the identification oftribes, genera and species, and also for morphs within species. The systematic accountincludes biological information and photomicrographs of each species. Wherever possibledistinguishing characters are provided that are amenable to the non-specialist, includingfield keys to aphids on conifers and plant roots.£35.00 plus postage and packaging; Members/Fellows receive 30% discount.Antenna 44(1).qxp_Layout 1  01/04/2020  14:36  Page 24View publication stats

New ways for old specimens - museomics is transforming the field of systematic entomology

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New ways for old specimens - museomics is transforming the field of systematic entomology

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