CC BY
12OECD+WoS: 1.06+IY (Entomology) https://doi.org/10.31993/2308-6459-2021-104-1-14945
Full-text article
IS APORIA CRATAEGI AN UNSUITABLE HOST OF WOLBACHIA SYMBIONTS?
R.A. Bykov*, G.V. Yurlova, M.A. Demenkova, Yu.Yu. Ilinsky
Institute of Cytology and Genetics SB RAS, Novosibirsk, Russia
*corresponding author, e-mail: bykovra@bionet.nsc.ru
The Black-veined White Aporia crataegi (Lepidoptera: Pieridae) is a trans-Palearctic species causing damage to various fruit and berry crops. Here we analyzed Wolbachia infection in A. crataegi populations. Wolbachia bacteria are maternally transmitted intracellular symbionts of many arthropods, including numerous Lepidoptera. We have studied 376 samples of A. crataegi collected in 10 regions of Russia from the Far East to Kaliningrad. Wolbachia prevalence was very low; only eight Wolbachia-positive specimens of A. crataegi were detected in Yakutia, Republic of Buyatia, Sverdlovsk and Kaliningrad Provinces, and no infection was found in other localities. Two Wolbachia haplotypes, ST-19 and ST-109, from A and B supergroups respectively, were identified using the multilocus sequence typing (MLST) protocol. These haplotypes were also previously reported in different lepidopteran species. Both Wolbachia haplotypes were associated with the same mtDNA haplotype (as inferred from the cytochrome oxidase subunit I gene) of A. crataegi, and ST-19 with two mtDNA haplotypes. This incongruence of maternally inherited agents indicates independent cases of the bacteria acquisition in A. crataegi history. The above data suggest that Wolbachia can infect Aporia crataegi but cannot establish in the host populations.
Keywords: Wolbachia, Pieridae, Lepidoptera, Aporia, mtDNA
Received: 10.01.2021 Accepted: 30.03.20211
Introduction
The Black-veined White Aporia crataegi L. (Lepidoptera: Pieridae) is a pest of various fruit and berry crops. The larvae damage the species of Prunus, Crataegus, Rosa, Pyrus, Padus, Sorbus and several other genera (Emmet, Heath 1989; Gorbunov, Kosterin, 2003). Population outbreaks result in complete defoliation of trees (Ilyinskiy, Tropin, 1965; Maximov, Marushchak, 2012). This butterfly is a trans-Palearctic species with high migratory activity (Tolman and Lewington 2008). The abundance of A. crataegi varies in different regions, for instance, in Russia it is rare in Ural, Amurland and Primorye, but abundant in most of West Siberia (Gorbunov, Kosterin, 2003). In some regions, populations of A. crataegi fluctuate greatly from year to year, e.g., in Ural (Gorbunov, Kosterin, 2003) or have long-term fluctuations, e.g., in Finland (Kuussaari et al. 2007). Decreasing A. crataegi populations (Fokin, Korovin, 2001; Kim et al., 2015; Jugovic et al., 2017), have been observed in the territories of Northern, Central, Eastern and Southern Europe, and North Africa, primarily due to human activity (van Swaay et al., 2010; Todisco et al., 2020). Extinction of A. crataegi has been reported in England, Czech Republic, The Netherlands, and South Korea (Asher et al. 2001; van Swaay et al., 2010; Park et al., 2013; Kim et al., 2020).
Bacteria of the Wolbachia genus are maternally inherited intracellular symbionts found in many insects (Hilgenboecker et al., 2008; Zug, Hammerstein, 2012). Wolbachia can affect host biology in different ways. Reproductive abnormalities, such as male killing, feminization of males, thelytokous parthenogenesis and cytoplasmic incompatibility (CI) are the ways for Wolbachia to spread in a host population (Werren et al., 2008). Wolbachia can also be a mutualist by providing
for essential nutrients, protecting from viruses and parasites or increasing lifespan and fecundity of the hosts (De Barro, Hart, 2001; Dong et al., 2007; Hosokawa et al., 2010; Nikoh et al., 2014; Van Nouhuys et al., 2016; Marino et al., 2017). Such deep involvement of the symbiont in the host biology allowed considering Wolbachia a potential agent for pest control (Zabalou et al., 2008; Bourtzis, 2008). Laboratory experiments of Wolbachia transmission from Rhagoletis cerasi (Diptera: Tephritidae) to Ceratitis capitata (Diptera: Tephritidae), an important agricultural pest, resulted in total progeny death due to complete CI in the new host (Zabalou et al., 2008). Transmission of CI-induced Wolbachia strain from Laodelphax striatellus (Hemiptera: Delphacidae) to a dangerous rice pest Nilaparvata lugens (Hemiptera: Delphacidae) results in high levels of CI as well, resulting in rice protection from Rice ragged stunt virus transmitted by the pest (Gong et al., 2020). However, most of such studies currently are limited to laboratory tests.
Wolbachia are divided into 17 phylogenetic clades, namely 'supergroups' which are denoted from A to S, excluding G and R (Werren et al., 1995; Lo et al., 2002; Baldo, Werren, 2007; Augustinos et al., 2011; Glowska et al., 2015; Gerth, 2016; Lefoulon et al., 2020). Supergroups A and B are the most common in insects, while the others are not so widespread, and some lineages are specific to the certain insect host taxa. The same Wolbachia variants could be found in hosts belonging to different taxa, which implies horizontal transmission (HT) of the symbiont (Werren 1997; Vavre et al., 1999; Dedeine et al., 2005; Haine et al., 2005; Stahlhut et al., 2010; Zug, Hammerstein, 2012; Ahmed et al., 2016; Ilinsky, Kosterin, 2017; Shaikevich et al., 2019). In spite of numerous cases of
© Bykov R.A., Yurlova G.V., Demenkova M.A., Ilinsky Yu.Yu., published by All-Russian Institute of Plant Protection (St. Petersburg). This is an open access article distributed under the terms of the Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
HT, maternal transmission within a host is rather stable, and the co-evolution of the symbiont and host mtDNA lineages is observed (Rousset, Solignac, 1995; Marcade et al., 1999; Hinrich et al., 2002; Mercot, Charlat., 2004; Shoemaker et al., 2004; Hurst, Jiggins, 2005; Ilinsky, 2013; Cariou et al., 2017; Chen et al., 2017). MtDNA of Wolbachia-infected species may undergo indirect selection that lead to reduction or increase in mtDNA diversity, changes in mtDNA variation, and to paraphyly of mtDNA (Hurst, Jiggins, 2005).
Wolbachia are found in a wide range of Lepidoptera species, and its prevalence greatly varies from low levels to totally infected populations (Tagami, Miura, 2004; Salunke et al., 2012; Ahmed et al., 2015; Solovyev et al., 2015; Ilinsky, Kosterin, 2017; Tokarev et al., 2017; Bykov et al., 2020; Malysh et al., 2020). Genetic diversity of Wolbachia in Lepidoptera hosts has been studied in detail employing the MLST protocol (Russell et al., 2009; Ahmed et al., 2016; Ilinsky, Kosterin, 2017; Duplouy et al., 2020). This protocol uses five bacterial loci: gatB, coxA, hcpA, ftsZ and fbpA; and a combination of alleles forms a Sequence Type (ST) or a haplotype (Baldo et al., 2006). Lepidopteran hosts often harbour Wolbachia strains
of ST-41 and other ST-41-related haplotypes which belong to the supergroup B (Ahmed et al., 2016; Ilinsky, Kosterin, 2017). Certain haplotypes of the supergroup A have been also found in Lepidoptera (Russell et al., 2009; Ahmed et al., 2016; Ilinsky, Kosterin, 2017; Duplouy et al., 2020). In some Lepidoptera, Wolbachia induce feminization, male killing, and CI (Hiroki et al., 2004; Charlat et al., 2006, 2007; Narita et al., 2007; Graham, Wilson, 2012; Salunkhe et al., 2014; Arai et al., 2019).
Previously, Wolbachia symbionts were found in some species of the Pieridae family, with high infection rates in Leptidea, Colias and Eurema species (Tagami, Miura, 2004; Solovyev et al., 2015; Ilinsky, Kosterin, 2017; Duplouy et al., 2020). For A. crataegi, Wolbachia infection was only noted in Novosibirsk population (see discussion in Ilinsky, Kosterin, 2017) without the data on the symbiont prevalence. Here, we analyzed Wolbachia prevalence in populations of A. crataegi throughout the Russian Federation from the Far East to Kaliningrad. Additionally, we studied mtDNA haplotypes and Wolbachia variants of A. crataegi to reveal their associations.
Materials and Methods
A total of 376 adults of A. crataegi were collected from 2001 to 2019 in 16 localities of 10 regions of Russian Federation from the Far East to Kaliningrad (Fig. 1; Table 1).
Total DNA was extracted from abdomens of air-dried or fresh samples in CTAB buffer by standard protocol (see Bykov et al., 2020). The DNA extraction quality was determined by PCR with the primer set HC02198/LC01490 (Vrijenhoek et al., 1994) for the mitochondrial cytochrome-c oxidase subunit 1 gene (COI). Wolbachia infection was examined by PCR with primers for coxA gene (Baldo et al., 2006). Six out of eight Wolbachia-positive samples were genotyped according to MLST protocol (Baldo et al., 2006). Additionally, we sequenced the 658 bp part of COI gene for these six Wolbachia-infected samples and eight uninfected
samples (one per region) to determine the mtDNA haplotypes of A. crataegi. Amplicons were purified with exonuclease I E. coli (New England Biolabs) and further were sequenced using BrilliantDye Terminator Cycle Sequencing kit v3.1 (Nimagen). All sequences were analyzed in FinchTV v1.4.0 (Geospiza Inc). All sequences were deposited to the GenBank database under accession numbers MW243570 - MW243583 for COI gene and MW246635 - MW246664 for MLST Wolbachia genes. The alignments were performed in MEGA 6 (Tamura et al., 2013). Phylogenetic reconstructions were performed in MEGA 6 by the maximum likelihood algorithm. The data on other populations of A. crataegi (Park et al., 2013; Kim et al., 2020; Todisco et al., 2020) with A. hippia as an outgroup taxon were used for mtDNA tree reconstruction.
Figure 1. Sampling sites for Aporia crataegi: 1 - Khabarovsk Krai; 2 - Yakutia, Oymyakonsky District; 3 - Yakutia, Yakutsk; 4 - Yakutia, Namsky District; 5 - Yakutia, Khangalassky District; 6 - Yakutia, Suntarsky District; 7 - Yakutia, Lensky District; 8 - Republic of Buryatia, Yeravninsky District; 9 - Republic of Buryatia, Khorinsky district; 10 - Altai Republic; 11 - Altai Krai; 12 - Kemerovo Province; 13 - Tomsk Province; 14 - Novosibirsk Province; 15 - Sverdlovsk Province; 16 - Kaliningrad Province. Dot size indicates sample size. Filled dots indicate localities where Wolbachia infection was found
Table 1. Wolbachia infection in populations
of Aporia crataegi
Region, locality Year N /N* w+
Khabarovsk Krai 2018 0/12
Yakutia, Oymyakonsky District 2017 0/1
Yakutia, Yakutsk 2003 2015 0/2 0/1
2002 0/1
Yakutia, Namsky District 2016 1/2
2017 0/1
Yakutia, Khangalassky District 2001 2016 0/4 0/1
Yakutia, Suntarsky District 2017 2/5
Yakutia, Lensky District 2012 0/4
Republic of Buryatia, Yeravninsky District 2018 0/1
Republic of Buryatia, Khorinsky district 2018 1/1
Kemerovo Province 2016 2017 0/4 0/15
Tomsk Province 2019 0/6
2016 0/67
Novosibirsk Province 2017 2018 0/49 0/2
2019 0/72
Altai Republic 2016 2017 0/4 0/15
Altai Krai 2017 2018 0/14 0/35
2015 1/20
Sverdlovsk Province 2016 2/20
2017 0/16
Kaliningrad Province 2017 1/1
Total: 8/376
* Nw+ - number Wolbachia-positive specimens; N - total number of analyzed insects.
Results
Screening of 376 A. crataegi specimens from the vast territory revealed only eight cases of Wolbachia infection (2 %). No specific geographic pattern of Wolbachia infection in populations of A. crataegi has been found. The symbiont has been detected in Yakutia, Republic of Buryatia, Sverdlovsk, and Kaliningrad Provinces (Table 1). In other regions, Wolbachia symbionts were not found even in large samples from Novosibirsk Province and Altai Krai.
Analysis of Wolbachia genetic diversity based on the MLST protocol revealed two haplotypes of the symbiont. Wolbachia ST-19 was found in samples from Yakutia, Sverdlovsk, and Kaliningrad Provinces, and ST-109 - in the sample from Buryatia. These haplotypes belonged to different Wolbachia supergroups: ST-19 - to A, and ST-109 - to B-supergroup (Fig. 2B).
We found discordance between mtDNA haplotypes of A. crataegi and Wolbachia haplotypes. Wolbachia haplotype ST-19 associated with two different mtDNA haplotypes of the host, and ST-109 - with one haplotype shared with ST-19 (Fig. 2A, B). One of these mtDNA haplotypes associated with Wolbachia haplotypes belongs to the most common and widespread «Eurasian» haplogroup (Todisco et al., 2020). This mtDNA haplotype was found in infected samples from Sverdlovsk and Kaliningrad Provinces and in uninfected samples from Novosibirsk, Kemerovo and Tomsk Provinces, Altai Krai, Republic of Buryatia and Altai Republic. The other mtDNA haplotype was found in infected and uninfected samples from Yakutia, and in uninfected samples from the Khabarovsk Krai. This haplotype belongs to the haplogroup previously described in Central and East Asia and Yakutia (Todisco et al., 2020), and it is probably typical for Asian populations of A. crataegi.
Discussion
Wolbachia prevalence in A. crataegi populations was very low. Similar cases oflow Wolbachia prevalence were previously described in Pieris rapae (Lepidoptera: Pieridae) populations, where 3.4 % infection prevalence was detected (Tagami, Miura, 2004). Possible explanation of such low Wolbachia prevalence may be the absence of any advantages given by the symbiont to its host and no reproductive abnormalities induced by Wolbachia. Besides, host immunity may be able to suppress the symbiont. There are species that are reported to be Wolbachia free based on hundreds of screened samples, such as Lymantria dispar (Lepidoptera: Lymantriidae) (Martemyanov et al., 2014; Ilinsky et al., 2017), Agriocnemis pygmaea (Odonata: Coenagrionidae) (Thipaksorn et al., 2003), Aedes caspius (Diptera: Culicidae) (Bozorg-Omid et al., 2020), Anopheles gambiae (Diptera: Culicidae) (Scholz et al., 2020). Reasons for Wolbachia absence in some species remain unclear.
In A. crataegi, we found two diverged Wolbachia haplotypes ST-19 and ST-109 that were also reported in different hosts. ST-109 (B supergroup) was found in Colotis amata (Pieridae), Minois dryas (Nymphalidae) and several Lycaenidae butterflies (Ahmed et al., 2016; Ilinsky, Kosterin, 2017). Haplotype ST-19 (A supergroup) was previously found in Pieridae, Pyralidae, Nymphalidae and Lycaenidae
buttrerflies (Russell et al., 2009; Ahmed et al., 2016; Ilinsky, Kosterin, 2017; Duplouy et al., 2020), and also reported for Coleoptera and different Hymenoptera species, including parasitic wasps of the Apanteles and Chelonus genera (Russell et al., 2009; Tseng et al., 2020; pubMLST database https:// pubmlst.org/organisms/wolbachia-spp). These wasps are parasitoids of different Lepidoptera, including A. crataegi (Wilbert, 1960); therefore, HT of Wolbachia between parasitic wasps and A. crataegi could not be ruled out. Reports of different Wolbachia supergroups in a single species are numerous (Tsutsui et al., 2003; Arthofer et al., 2009; Chai, Duo, 2011; Wiwatanaratanabutr, Zhang, 2016; Duplouy, Brattström 2018). For instance, in Homona magnanima (Lepidoptera: Tortricidae) there were three Wolbachia strains, two from the supergroup A and one from the supergroup B (Arai et al., 2019).
Long-term Wolbachia-host association leads to a specific pattern of Wolbachia variants and mitochondrial DNA. When a particular Wolbachia variant is coinherited with a particular maternal lineage, co-cladogenesis of these inherited factors could be observed. Recent Wolbachia acquisitions would not demonstrate any specific pattern of coinheritance. Assuming the co-evolution of Wolbachia and host mtDNA, we expected to find similar mtDNA haplotypes in A. crataegi specimens
Figure 2. (A) - Maximum likelihood (ML) tree of A. crataegi mtDNA was reconstructed using the Tamura 3-parameter model of nucleotide replacement based on the 658bp region of the COI gene. Regions of collection are indicated. Samples investigated in this study are indicated in bold. Wolbachia-infected samples are indicated with (+); (B) - The ML tree of Wolbachia haplotypes was reconstructed based on concatenated sequences of five MLST genes using the GTR model of nucleotide replacement. Host species and Wolbachia haplotypes (STs) are indicated. Studied haplotypes ST-19 and -109 are in bold. Seven Wolbachia haplotypes (ST-1, -8, -9, -35, -41, -62, and -90) were used as references for the supergroups. Associations of Wolbachia haplotypes with mtDNA haplotypes of A. crataegi are indicated. Bootstrap values higher then 75 (1000 replicates)
are indicated on both trees
infected with the same Wolbachia haplotype. However, two symbiont haplotypes were linked to the same host mtDNA haplotype and different mtDNA haplotypes co-occurred with ST-19 Wolbachia haplotype. Those Wolbachia haplotypes
belonged to supergroups A and B, which diverged 58-200 Mya (Werren et al., 1995; Gerth, Bleidorn, 2017). Thus, we suppose that Wolbachia has recently emerged in A. crataegi populations.
Conclusion
Our data showed that widespread Wolbachia variants has recently infected A. crataegi, as inferred from the incongruence of Wolbachia and host mtDNA haplotypes.
Low Wolbachia prevalence might indicate the difficulty of the symbiont establishment in A. crataegi populations, suggesting that A. crataegi is not a suitable host of Wolbachia.
Acknowledgments
The study was funded by the Russian Foundation for Basic Research (grants # 18-316-00099 and 19-04-00983)
and the State Budgeted Project #0259-2021-0016*. The authors express sincere gratitude to our colleagues who collected and kindly provided us with material from different regions: V.V. Dubatolov (Institute of Systematics and Ecology of Animals, SB RAS) - from the Khabarovsk Krai; S.V. Shehovtsov (Institute of Cytology and Genetics, SB RAS) - from the Republic of Buyatia;
I.A. Kerchev (Institute of Systematics and Ecology of Animals, SB RAS) - from Tomsk; A.P. Burnasheva (Institute for Biological Problems of Cryolithozone, SB RAS) - from Yakutia; I.A. Solonkin and E.Yu. Zakharova (Institute of Plant and Animal Ecology, UB RAS) - from Sverdlovsk Province, and to O.E. Kosterin (Institute of Cytology & Genetics, SB RAS) - from Novosibirsk.
*acknowledgment of project # 0259-2021-0016 is lacking in the hardcopy version of the manuscript due to technical reasons
References
Ahmed MZ, Araujo-Jnr EV, Welch JJ, Kawahara AY (2015) Wolbachia in butterflies and moths: geographic structure in infection frequency. Front Zool 12 (1):1-16. https://doi. org/10.1186/s12983-015-0107-z Ahmed MZ, Breinholt JW, Kawahara AY (2016) Evidence for common horizontal transmission of Wolbachia among butterflies and moths. BMC Evol Biol 16(1):1-16. https:// doi.org/10.1186/s12862-016-0660-x Arai H, Hirano T, Akizuki N, Abe A et al (2019) Multiple infection and reproductive manipulations of Wolbachia in Homona magnanima (Lepidoptera: Tortricidae). Microb Ecol 77(1):257-266. https://doi.org/10.1007/s00248-018-1210-4 Arthofer W, Riegler M, Avtzis DN, Stauffer C (2009) Evidence for low-titre infections in insect symbiosis: Wolbachia in the bark beetle Pityogenes chalcographus (Coleoptera, Scolytinae). Environ Microbiol 11(8):1923-1933. https:// doi.org/ 10.1111/j.1462-2920.2009.01914.x Asher J, Warren M, Fox R, Harding P et al (2001) The millennium atlas of butterflies in Britain and Ireland. Oxford University Press. Augustinos AA, Santos-Garcia D, Dionyssopoulou E, Moreira M et al (2011) Detection and characterization of Wolbachia infections in natural populations of aphids: is the hidden diversity fully unraveled? PloS One 6(12):e28695. https:// doi.org/10.1371/journal.pone.0028695 Baldo L, Hotopp JCD, Jolley KA, Bordenstein SR et al (2006) Multilocus sequence typing system for the endosymbiont Wolbachia pipientis. Appl Environ Microbiol 72(11):7098-7110. https://doi.org/10.1128/AEM.00731-06 Baldo L, Werren JH (2007) Revisiting Wolbachia supergroup typing based on WSP: spurious lineages and discordance with MLST. Curr Microbiol 55(1):81-87. https://doi. org/10.1007/s00284-007-0055-8 Bourtzis K (2008) Wolbachia-based technologies for insect pest population control. Transgenesis and the management of vector-borne disease 104-113. Bozorg-Omid F, Oshaghi MA, Vahedi M, Karimian F et al (2020) Wolbachia infection in West Nile Virus vectors of northwest Iran. Appl Entomol Zool 55(1):105-113. https:// doi.org/10.1007/s13355-019-00658-6 Bykov RA, Yudina MA, Gruntenko NE, Zakharov IK et al (2019) Prevalence and genetic diversity of Wolbachia endosymbiont and mtDNA in Palearctic populations of Drosophila melanogaster. BMC Evol Biol 19(1):45-53. https://doi.org/10.1186/s12862-019-1372-9 Bykov RA, Yurlova GV, Demenkova MA, Dubatolov VV et al (2020) [High Wolbachia prevalence in populations of Siberian silk moth Dendrolimus superans sibiricus Tschetverikov, 1908 (Lepidoptera: Lasiocampidae) in the territory of Russia]. Zhurnal obshchey biologii 81(5):387-393. (In Russian). https://doi.org/10.31857/ S0044459620050036 Cariou M, Duret L, Charlat S (2017) The global impact of Wolbachia on mitochondrial diversity and evolution. J Evol Biol 30(12):2204-2210. https://doi.org/10.1111/jeb.13186 Chai HN, Du YZ (2011) Detection and phylogenetic analysis of Wolbachia wsp in the Chilo suppressalis (Lepidoptera: Crambidae) in China. Ann Entomol Soc Am 104(5):998-1004. https://doi.org/10.1603/AN11072
Charlat S, Engelstädter J, Dyson EA, Hornett EA et al (2006) Competing selfish genetic elements in the butterfly Hypolimnas bolina. Curr Biol 16(24):2453-2458. https:// doi.org/10.1016/j.cub.2006.10.062 Charlat S, Hornett EA, Fullard JH, Davies NR et al (2007) Extraordinary flux in sex ratio. Science 317(5835):214-214. https://doi.org/10.1126/science.1143369 Chen F, Coates B, He KL, Bai SX et al (2017) Effects of Wolbachia on mitochondrial DNA variation in populations of Athetis lepigone (Lepidoptera: Noctuidae) in China. Mitochondrial DNA Part A 28(6):826-834. https://doi.org/ 10.1080/24701394.2016.1197216 Chu D, Gao CS, De Barro P, Zhang YJ et al (2011) Further insights into the strange role of bacterial endosymbionts in whitefly, Bemisia tabaci: Comparison of secondary symbionts from biotypes B and Q in China. Bull Entomol Res 101(4):477. https://doi.org/10.1017/S0007485311000083 De Barro PJ, Hart PJ (2001) Antibiotic curing of parthenogenesis in Eretmocerus mundus (Australian parthenogenic form). Entomol Exp Appl 99:225-230. https:// doi.org/10.1046/j.1570-7458.2001.00821.x Dedeine F, Ahrens M, Calcaterra L, Shoemaker DD (2005) Social parasitism in fire ants (Solenopsis spp.): a potential mechanism for interspecies transfer of Wolbachia. Mol Ecol 14(5):1543-1548. https://doi. org/10.1111/j.1365-294X.2005.02499.x Dong P, Wang JJ, Hu F, Jia FX (2007) Influence of Wolbachia infection on the fitness of the stored-product pest Liposcelis tricolor (Psocoptera: Liposcelididae). J Econ Entomol 100:1476-1481. https://doi.org/10.1093/jee/100.4.1476 Duplouy A, Brattström O (2018) Wolbachia in the genus Bicyclus: a forgotten player. Microb Ecol 75(1):255-263. https://doi.org/10.1007/s00248-017-1024-9 Duplouy A, Pranter R, Warren-Gash H, Tropek R et al (2020) Towards unravelling Wolbachia global exchange: a contribution from the Bicyclus and Mylothris butterflies in the Afrotropics. BMC Microbiol 20(1):1-9. https://doi. org/10.1186/s12866-020-02011-2 Emmet AM, Heath J (1989) The moths and butterflies of Great
Britain and Ireland, vol 7, part 1. Harley Books Fokin AV, Korovin AA (2001) [Effect of biopreparations on trophic activity of caterpillars of lackey moth and pierid butterfly]. Zashchita i Karantin Rastenii5:20 (In Russian) Gerth M (2016) Classification of Wolbachia (Alphaproteobacteria, Rickettsiales): No Evidence for a Distinct Supergroup in Cave Spiders. Infect Genet Evol 43:378-380. https://doi.org/10.1101/046169 Glowska E, Dragun-Damian A, Dabert M, Gerth M (2015) New Wolbachia supergroups detected in quill mites (Acari: Syringophilidae). Infect Genet Evol 30:140-146. https://doi. org/10.1016/j.meegid.2014.12.019 Gorbunov PI, Kosterin OE (2007) The butterflies (Hesperioidea and Papilionoidea) of North Asia (Asian part of Russia) in nature (Vol. 2). Rodina & Fodio. 408 p. Gong JT, Li Y, Li TP, Liang Y et al (2020) Stable introduction of plant-virus-inhibiting Wolbachia into planthoppers for rice protection. Curr Biol 30(24):4837-4845. https://doi. org/10.1016/j.cub.2020.09.033 Graham RI, Wilson K (2012) Male-killing Wolbachia and mitochondrial selective sweep in a migratory
African insect. BMC Evol Biol 12(1):204. https://doi. org/10.1186/1471-2148-12-204 Haine ER, Pickup NJ, Cook JM (2005) Horizontal transmission of Wolbachia in a Drosophila community. Ecol Entomol 30(4):464-472. https://doi. org/10.1111/j.0307-6946.2005.00715.x Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A et al (2008) How many species are infected with Wolbachia?-a statistical analysis of current data. FEMS Microbiol Lett 281(2):215-220. https://doi. org/10.1111/j.1574-6968.2008.01110.x Hinrich J, Vd Schulenburg G, Hurst GD, Tetzlaff D et al (2002) History of infection with different male-killing bacteria in the two-spot ladybird beetle Adalia bipunctata revealed through mitochondrial DNA sequence analysis. Genetics 160(3):1075-1086. https://doi.org/10.1093/ genetics/160.3.1075 Hiroki M, Tagami Y, Miura K, Kato Y (2004) Multiple infection with Wolbachia inducing different reproductive manipulations in the butterfly Eurema hecabe. Proc R Soc Lond B Biol Sci 271(1549):1751-1755. https://doi. org/10.1098/rspb.2004.2769 Hosokawa T, Koga R, Kikuchi Y, Meng XY et al (2010) Wolbachia as a bacteriocyte-associated nutritional mutualist. Proc Natl Acad Sci USA 107:769-774. https://doi. org/10.1073/pnas.0911476107 Hurst GD, Jiggins FM (2005) Problems with mitochondrial DNA as a marker in population, phylogeographic and phylogenetic studies: the effects of inherited symbionts. Proc R Soc Lond B Biol Sci 272(1572):1525-1534. https:// doi.org/10.1098/rspb.2005.3056 Ilyinskiy AI, Tropin IV (1965) [Surveillance, Registration, and Prognosis of Mass Growth of Needle and Leaf Eating Insects in the Forests of the USSR]. Moscow: Lesnaya Promyshlennost. 525 p. (In Russian). Ilnsky Y (2013) Coevolution of Drosophila melanogaster mtDNA and Wolbachia genotypes. PLoS One 8(1):e54373. https://doi.org/10.1371/journal.pone.0054373 Ilinsky Y, Kosterin OE (2017) Molecular diversity of Wolbachia in Lepidoptera: prevalent allelic content and high recombination of MLST genes. Mol Phylogenet Evol 109:164-179. https://doi.org/10.1016Zj.ympev.2016.12.034 Ilinsky YY, Tokarev YS, Bykov RA, Yudina MA et al (2017) Detection of bacterial symbionts (Wolbachia, Spiroplasma) and eukaryotic pathogen (Microsporidia) in Japanese populations of gypsy moth species (Lymantria spp.). Evraziatskiy Entomologicheskiy Zhurnal 16(1):1-5. Jing LI, Wang ZY, Bourguet D, He KL (2013) Wolbachia infection in populations of Ostrinia furnacalis: diversity, prevalence, phylogeny and evidence for horizontal transmission. J Integr Agric 12(2):283-295. https://doi. org/10.1016/S2095-3119(13)60227-0 Jugovic J, Crne M, Luznic M (2017) Movement, demography and behaviour of a highly mobile species: A case study of the black-veined white, Aporia crataegi (Lepidoptera: Pieridae). Eur J Entomol 114:113-122. https://doi.org/10.14411/ eje.2017.016
Kawasaki Y, Schuler H, Stauffer C, Lakatos F, Kajimura H (2016) Wolbachia endosymbionts in haplodiploid and diploid scolytine beetles (Coleoptera: Curculionidae:
Scolytinae). Environ Microbiol Rep 8(5):680-688. https:// doi.org/10.1111/1758-2229.12425 Kim TG, Han YG, Kwon O, Cho Y (2015) Changes in Aporia crataegi's potential habitats in accordance with climate changes in the northeast Asia. J Ecol Environ 38(1):15-23. https://doi.org/10.5141/ecoenv.2015.002 Kim MJ, Cho Y, Wang AR, Kim SS et al (2020) Population genetic characterization of the black-veined white, Aporia crataegi (Lepidoptera: Pieridae), using novel microsatellite markers and mitochondrial DNA gene sequences. Conserv Genet 21(2):359-371. https://doi.org/10.1007/ s10592-020-01257-7 Kuussaari M, Heliölä J, Pöyry J, Saarinen K (2007) Contrasting trends of butterfly species preferring semi-natural grasslands, field margins and forest edges in northern Europe. J Insect Conserv 11(4):351-366. https:// doi.org/10.1007/s10841-006-9052-7 Lefoulon E, Clark T, Borveto F, Perriat-Sanguinet M et al (2020) Pseudoscorpion Wolbachia symbionts: diversity and evidence for a new supergroup S. BMC Microbiol 20(1):1-15. https://doi.org/10.1186/s12866-020-01863-y Lo N, Casiraghi M, Salati E, Bazzocchi C, Bandi C (2002) How many Wolbachia supergroups exist? Mol Biol Evol 19(3):341-346. https://doi.org/10.1093/oxfordjournals. molbev.a004087 Malysh JM, Malysh SM, Kireeva DS, Kononchuk AG et al (2020) Detection of Wolbachia in larvae of Loxostege sticticalis (Pyraloidea: Crambidae) in European and Asian parts of Russia. Plant Protection News 1:49-52. https://doi. org/10.31993/2308-6459-2020-103-1-49-52 Marcade I, Souty-Grosset C, Bouchon D, Rigaud T, Raimond R (1999) Mitochondrial DNA variability and Wolbachia infection in two sibling woodlice species. Heredity 83(1):71-78. https://doi.org/10.1038/sj.hdy.6885380 Marino Y, Rodrigues VJ, Bayman P (2017) Wolbachia affects reproduction and population dynamics of the coffee berry borer (Hypothenemus hampei): Implications for biological control. Insects 8(1):8. https://doi.org/10.3390/ insects8010008 Martemyanov VV, Iudina MA, Belousova IA, Bykov RA, Ilinsky YuYu (2014) [The screening of Wolbachia infection in gypsy moth (Lymantria dispar) populations in Siberia] Evraziatskiy Entomologicheskiy Zhurnal 13(5):494-496 (In Russian).
Maximov SA, Marushchak VN (2012) [Towards reasons of outbreaks of the Black-veined White in the Ural] Agrarnyy vestnik Urala 11(103):28-30 (In Russian). Mergot H, Charlat S (2004) Wolbachia infections in Drosophila melanogaster and D. simulans: polymorphism and levels of cytoplasmic incompatibility. Genetica 120:51-59. https:// doi.org/10.1023/b:gene.0000017629.31383.8f Narita S, Kageyama D, Nomura M, Fukatsu T (2007) Unexpected mechanism of symbiont-induced reversal of insect sex: feminizing Wolbachia continuously acts on the butterfly Eurema hecabe during larval development. Appl Environ Microbiol 73(13):4332-4341. https://doi. org/10.1128/AEM.00145-07 Nikoh N, Hosokawa T, Moriyama M, Oshima K (2014) Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc Natl Acad Sci USA 111:10257-10262. https://doi.org/10.1073/pnas.1409284111
Park HC, Han T, Kang TW, Yi DA et al (2013) DNA barcode analysis for conservation of an endangered species, Aporia crataegi (Lepidoptera, Pieridae) in Korea. Journal of Sericultural and Entomological Science 51(2):201-206. https://doi.org/10.7852/jses.2013.5L2.201 Rousset F, Solignac M (1995) Evolution of single and double Wolbachia symbioses during speciation in the Drosophila simulans complex. Proc Natl Acad Sci USA 92(14):6389-6393. https://doi.org/10.1073/pnas.92.14.6389 Russell JA, Goldman-Huertas B, Moreau CS, Baldo L et al (2009) Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63(3):624-640. https://doi. org/10.1111/j.1558-5646.2008.00579.x Solovyev VI, Ilinsky Y, Kosterin OE (2015) Genetic integrity of four species of Leptidea (Pieridae, Lepidoptera) as sampled in sympatry in West Siberia. Comp Cytogenet 9(3):299. https://doi.org/10.3897/CompCytogen.v9i3.4636 Salunke BK, Salunkhe RC, Dhotre DP, Walujkar SA et al (2012) Determination of Wolbachia diversity in butterflies from Western Ghats, India, by a multigene approach. Appl Environ Microbiol 78(12):4458-4467. https://doi. org/10.1128/AEM.07298-11 Salunkhe RC, Narkhede KP, Shouche YS (2014) Distribution and evolutionary impact of Wolbachia on butterfly hosts. Ind J Microbiol 54(3):249-254. https://doi.org/10.1007/ s12088-014-0448-x Sazama EJ, Bosch MJ, Shouldis CS, Ouellette SP et al (2017) Incidence of Wolbachia in aquatic insects. Ecol Evol 7(4):1165-1169. https://doi.org/10.1002/ece3.2742 Scholz M, Albanese D, Tuohy K, Donati C et al (2020). Large scale genome reconstructions illuminate Wolbachia evolution. Nat Commun 11(1):1-11. https://doi.org/10.1038/ s41467-020-19016-0 Shaikevich E, Bogacheva A, Rakova V, Ganushkina L et al (2019) Wolbachia symbionts in mosquitoes: Intra-and intersupergroup recombinations, horizontal transmission and evolution. Mol Phylogenet Evol 134:24-34. https://doi. org/10.1016/j.ympev.2019.01.020 Shoemaker DD, Dyer KA, Ahrens M, McAbee K, Jaenike J (2004) Decreased diversity but increased substitution rate in host mtDNA as a consequence of Wolbachia endosymbiont infection. Genetics 168(4):2049-2058. https://doi. org/10.1534/genetics.104.030890 Stahlhut JK, Desjardins CA, Clark ME, Baldo L et al (2010) The mushroom habitat as an ecological arena for global exchange of Wolbachia. Mol Ecol 19(9):1940-1952. https:// doi.org/10.1111/j.1365-294X.2010.04572.x Tagami Y, Miura K (2004) Distribution and prevalence of Wolbachia in Japanese populations of Lepidoptera. Insect Mol Biol 13(4):359-364. https://doi. org/10.1111/j.0962-1075.2004.00492.x Tamura K, Stecher G, Peterson D, Filipski A et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725-2729. https://doi.org/10.1093/ molbev/mst197
Thipaksorn A, Jamnongluk W, Kittayapong P (2003) Molecular evidence of Wolbachia infection in natural populations of tropical odonates. Curr Microbiol 47(4):0314-0318. https:// doi.org/10.1007/s00284-002-4010-4
Todisco V, Vodä R, Prosser SW, Nazari V (2020) Next generation sequencing-aided comprehensive geographic coverage sheds light on the status of rare and extinct populations of Aporia butterflies (Lepidoptera: Pieridae). Sci Rep 10(1):1-9. https://doi.org/10.1038/s41598-020-70957-4 Tokarev YS, Yudina MA, Malysh JM, Bykov RA et al (2018) Prevalence Rates of the Endosymbiotic Bacterium of the Wolbachia Genus in Natural Populations of Ostrinia nubilalis and Ostrinia scapulalis (Lepidoptera: Pyraloidea: Crambidae) in Southwestern Russia. Russian Journal of Genetics: Applied Research 8(2):172-177. https://doi. org/10.1134/S2079059718020119 Tolman T, Lewington R (2008) Collins butterfly guide. Harper
Collins Publishers Ltd., London, p 384 Tseng SP, Hsu PW, Lee CC, Wetterer JK et al (2020) Evidence for Common Horizontal Transmission of Wolbachia among Ants and Ant Crickets: Kleptoparasitism Added to the List. Microorganisms 8(6):805. https://doi.org/10.3390/ microorganisms8060805 Tsutsui ND, Kauppinen SN, Oyafuso AF, Grosberg RK (2003) The distribution and evolutionary history of Wolbachia infection in native and introduced populations of the invasive argentine ant (Linepithema humile). Mol Ecol 12(11):3057-3068. https://doi.org/10.1046/j.1365-294X.2003.01979.x Van Nouhuys S, Kohonen M, Duplouy A (2016) Wolbachia increases the susceptibility of a parasitoid wasp to hyperparasitism. J Exp Biol 219:2984-2990. https://doi. org/10.1242/jeb.140699 van Swaay C et al. Aporia crataegi. The IUCN Red List of Threatened Species (2010) https://www.iucnredlist.org (10.11.2019)
Vavre F, Fleury F, Lepetit D, Fouillet P, Boulétreau M (1999) Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16(12):1711-1723. https://doi.org/10.1093/oxfordjournals. molbev.a026084 Verspoor RL, Haddrill PR (2011) Genetic diversity, population structure and Wolbachia infection status in a worldwide sample of Drosophila melanogaster and D. simulans populations. PLoS One. 6(10):e26318. https://doi. org/10.1371/journal.pone.0026318 Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3(5):294-299.
Weinert LA, Tinsley MC, Temperley M, Jiggins FM (2007) Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol Lett 3(6):678-681. https://doi.org/10.1098/rsbl.2007.0373 Werren JH, Zhang W, Guo LR (1995) Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc R Soc Lond B Biol Sci 261(1360):55-63. https://doi. org/10.1098/rspb.1995.0117 Werren JH (1997) Biology of Wolbachia. Annu Rev Entomol 42(1):587-609.
Werren JH, Windsor DM (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proc R Soc Lond B Biol Sci 267(1450):1277-1285. https:// doi.org/10.1098/rspb.2000.1139
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6(10):741-751. https://doi.org/10.1038/nrmicro1969 Wilbert EL (1960) Apanteles pieridis a parasite of Aporia
crataegi. Entomophaga 5(3):183-211 Wiwatanaratanabutr I, Zhang C (2016) Wolbachia infections in mosquitoes and their predators inhabiting rice field communities in Thailand and China. Acta tropica 159:153— 160. https://doi.org/10.1016/j.actatropica.2016.03.026
Вестник защиты растений, 2021, 104(1), с. OECD+WoS: 1.06+IY (Entomology)
Zabalou S, Riegler M, Theodorakopoulou M, Stauffer C et al (2004) Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc Natl Acad Sci USA 101(42):15042-15045. https://doi.org/10.1073/ pnas.0403853101 Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PloS One 7(6):e38544. https://doi.org/10.1371/journal.pone.0038544
https://doi.org/10.31993/2308-6459-2021-104-1-14945 Полнотекстовая статья
APORIA CRATAEGI НЕУДОБНЫЙ ХОЗЯИН ДЛЯ WOLBACHIA?
Р.А. Быков*, Г.В. Юрлова, М.А. Деменкова, Ю.Ю. Илинский
Институт цитологии и генетики СО РАН, Новосибирск
*ответственный за переписку, e-mail: bykovra@bionet.nsc.ru
Боярышница Aporia crataegi (Lepidoptera: Pieridae) - Транспалеарктический вид, который вредит различным плодово-ягодным культурам. Мы проводим анализ инфицированности Wolbachia популяций A. crataegi. Бактерии Wolbachia - это матерински-наследуемые внутриклеточные симбионты многих членистоногих, в том числе Чешуекрылых. Мы изучили 376 образцов A. crataegi, собранных в 10 регионах России от Дальнего Востока до Калининграда. Частота встречаемости Wolbachia была очень низкой, только восемь Wolbachia-положительных образцов A. crataegi было обнаружено в Якутии, Республике Бурятия, Свердловской и Калининградской областях, и не было выявлено инфекции в других локалитетах. Два гаплотипа Wolbachia, ST-19 и ST-109, из A и B супергрупп соответственно, были определены с использованием протокола мультилокусного генотипирования (MLST). Эти гаплотипы также встречаются у разных видов чешуекрылых. Оба гаплотипа Wolbachia ассоциированы с одним гаплотипом мтДНК A. crataegi (определенным на основании анализа гена первой субъединицы цитохром с-оксидазы), а ST-19 - с двумя гаплотипами мтДНК. Это несоответствие матерински наследуемых агентов указывает на случаи независимого приобретения бактерий в истории A. crataegi. Все вышеперечисленные данные позволяют предположить, что Wolbachia может инфицировать Aporia crataegi, но не способна закрепиться в популяциях хозяина.
Ключевые слова: Wolbachia, Pieridae, Lepidoptera, Aporia, мтДНК
Поступила в редакцию: 10.01.2021
Принята к печати: 30.03.2021
© Быков Р.А., Юрлова Г.В., Деменкова М.А., Илинский Ю.Ю. Статья открытого доступа,
публикуемая Всероссийским институтом защиты растений (Санкт-Петербург) и распространяемая на условиях Creative Commons Attribution License 4.0 (http://creativecommons.org/licenses/by/4.0/).
