Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Secondary contact zone and genetic introgression in closely related haplodiploid social spider mites

Heredity (2024)Cite this article

Subjects

Abstract

How frequently hybridisation and gene flow occur in the contact zones of diverging taxa is important for understanding the speciation process. Stigmaeopsis sabelisi and Stigmaeopsis miscanthi high-aggression form (hereafter, S. miscanthi HG) are haplodiploid, social spider mites that infest the Chinese silver grass, Miscanthus sinensis. These two species are closely related and parapatrically distributed in Japan. In mountainous areas, S. sabelisi and S. miscanthi HG are often found in the highlands and lowlands, respectively, suggesting that they are in contact at intermediate altitudes. It is estimated that they diverged from their common ancestors distributed in subtropical regions (south of Japan) during the last glacial period, expanded their distribution into the Japanese Archipelago, and came to have such a parapatric distribution (secondary contact). As their reproductive isolation is strong but incomplete, hybridisation and genetic introgression are expected at their distributional boundaries. In this study, we investigated their spatial distribution patterns along the elevation on Mt. Amagi using male morphological differences, and investigated their hybridisation status using single-nucleotide polymorphisms by MIG-seq. We found their contact zone at altitudes of 150–430 m, suggesting that their contact zone is prevalent in the parapatric area, which is in line with a previous study. Interspecific mating was predicted based on the sex ratio in the contact zone. No obvious hybrids were found, but genetic introgression was detected although it was extremely low.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The geographic distribution of the social spider mite Stigmaeopsis miscanthi species group in and around the Japanese Archipelago.
Fig. 2: Distributional patterns of S. sabelisi and S. miscanthi HG along altitude in both sexes based on the discriminant scores in the species identification by male morphology.
Fig. 3: The third leg of a normal and abnormal males.
Fig. 4: Sex ratio (proportion of males) in mite colonies along altitude.
Fig. 5: Neighbor-Net network of S. miscanthi species group collected from Mt. Amagi.
Fig. 6: Population genetic structure in mite colonies along altitude.

Similar content being viewed by others

Data availability

All raw reads of the MIG-seq data are available from the DDBJ Sequence Read Archive under BioProject ID PRJDB17427. The morphology, sex ratio, and cross-experimental data are shown in the Supplementary Materials.

References

  • Abbott R, Albach D, Ansell S, Arntzen JW, Baird SJE, Bierne N et al. (2013) Hybridization and speciation. J Evolut Biol 26:229–246

    Article  CAS  Google Scholar 

  • Belliure B, Montserratv M, Magalhães S (2010) Mites as models for experimental evolution studies. Acarologia 50:513–529

    Article  Google Scholar 

  • Blackmon H, Hardy NB, Laura R (2015) The evolutionary dynamics of haplodiploidy: Genome architecture and haploid viability. Evolution 69:2971–2978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boubou A, Migeon A, Roderick GK, Auger P, Cornuet J-M, Magalhes S, Navajas M (2012) Test of colonisation scenarios reveals complex invasion history of the red tomato spider mite Tetranychus evansi. PLoS ONE 7:e35601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clark LV, Brummer JE, Głowacka K, Hall MC, Heo K, Peng J et al. (2014) A footprint of past climate change on the diversity and population structure of Miscanthus sinensis. Ann Bot 114:97–107

    Article  PubMed  PubMed Central  Google Scholar 

  • Coyne JA, Orr HA (2004). Speciation, 1st edition. Sinauer Associates, Inc.: Sunderland, Mass

  • Dobzhansky T (1959) Genetics and the Origin of Species, Third Edition. Columbia University Press

  • Earl DA, von Holdt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361

    Article  Google Scholar 

  • Edelman NB, Frandsen PB, Miyagi M, Clavijo B, Davey J, Dikow RB et al. (2019) Genomic architecture and introgression shape a butterfly radiation. Science 366:594–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardy ICW (2002) Sex Ratios: Concepts and Research Methods. Cambridge University Press

  • Hoskin CJ, Higgie M, McDonald KR, Moritz C (2005) Reinforcement drives rapid allopatric speciation. Nature 437:1353–1356

    Article  CAS  PubMed  Google Scholar 

  • Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363

    Article  PubMed  Google Scholar 

  • Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267

    Article  CAS  PubMed  Google Scholar 

  • Johannesson K, Le Moan A, Perini S, André C (2020) A Darwinian Laboratory of Multiple Contact Zones. Trends Ecol Evolut 35:1021–1036

    Article  Google Scholar 

  • Knegt B, Potter T, Pearson NA, Sato Y, Staudacher H, Schmmel BCJ, Kiers ET, Egas M (2017) Detection of genetic incompatibilities in non-model systems using simple genetic markers: hybrid breakdown in the haplodiploid spider mite Tetranychus evansi. Heredity 118:311–321

    Article  CAS  PubMed  Google Scholar 

  • Lohse K, Ross L (2015) What haplodiploids can teach us about hybridization and speciation. Mol Ecol 20:5075–5077

    Article  Google Scholar 

  • Macke E, Magalhães S, Khan HD-T, Luciano A, Facon B, Olivieri I (2010) Sex allocation in haplodiploids is mediated by egg size: evidence in the spider mite Tetranychus urticae Koch. Proc R Soc B: Biol Sci 278:1054–1063

    Article  Google Scholar 

  • Mallet J (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc B: Biol Sci 363:2971–2986

    Article  Google Scholar 

  • Mayr E (1963) Animal species and evolution. Belknap Press

  • Nouhaud P, Blanckaert A, Bank C, Kulmuni J (2020) Understanding admixture: Haplodiploidy to the rescue. Trends Ecol Evolut35:34–42

    Article  Google Scholar 

  • Pfennig KS, Rice AM (2014) Reinforcement generates reproductive isolation between neighbouring conspecific populations of spadefoot toads. Proc R Soc Lond B: Biol Sci 281:20140949

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • R Core Team (2024). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria

  • Rieseberg LH (1997) Hybrid origins of plant species. Annu Rev Ecol Syst 28:359–389

    Article  Google Scholar 

  • Rochette NC, Rivera-Colón AG, Catchen JM (2019) Stacks 2: Analytical methods for paired-end sequencing improve RADseq-based population genomics. Mol Ecol 28:4737–4754

    Article  CAS  PubMed  Google Scholar 

  • Saitō Y (1986a) Prey kills predator: Counter-attack success of a spider mite against its specific phytoseiid predator. Exp Appl Acarol 2:47–62

    Article  Google Scholar 

  • Saitō Y (1986b) Biparental defence in a spider mite (Acari: Tetranychidae) infesting Sasa bamboo. Behav Ecol Sociobiol 18:377–386

    Article  Google Scholar 

  • Saitō Y (1990) ‘Harem’ and ‘non-harem’ type mating systems in two species of subsocial spider mites (Acari, Tetranychidae). Res. Popul Ecol 32:263–278

    Article  Google Scholar 

  • Saito Y (1995) Clinal variation in male-to-male antagonism and weaponry in a subsocial mite. Evolution 49:413–417

    Article  Google Scholar 

  • Saito Y (2010). Plant Mites and Sociality: Diversity and Evolution. Springer Science & Business Media

  • Saito Y (2011) Spider mites as study objects for evolutionary biology. In: Sabelis MW and Bruin J (eds) Trends in Acarology: Proceedings of the 12th International Congress, Springer, pp. 287-293

  • Saito Y, Chittenden AR, Kanazawa M (2011) Counterattack success of a social spider mite against two predominant phytoseiid predator species. Exp Appl Acarol 55:249

    Article  PubMed  Google Scholar 

  • Saito Y, Kanazawa M, Sato Y (2013) Life history differences between two forms of the social spider mite, Stigmaeopsis miscanthi. Exp Appl Acarol 60:313–320

    Article  PubMed  Google Scholar 

  • Saito Y, Sahara K (1999) Two clinal trends in male-male aggressiveness in a subsocial spider mite (Schizotetranychus miscanthi). Behav Ecol Sociobiol 46:25–29

    Article  Google Scholar 

  • Saito Y, Sakagami T, Sahara K (2002) Differences in diapause attributes between two clinal forms distinguished by male-to-male aggression in a subsocial spider mite, Schizotetranychus miscanthi Saito. Ecol Res 17:645–653

    Article  Google Scholar 

  • Saito Y, Sato Y, Chittenden AR, Lin J-Z, Zhang Y-X (2018) Description of two new species of Stigmaeopsis, Banks 1917 (Acari, Tetranychidae) inhabiting Miscanthus grasses (Poaceae). Acarologia 58:414–429

    Article  Google Scholar 

  • Saito Y, Sato Y, Kongchuensin M, Chao J-T, Sahara K (2019) New Stigmaeopsis species on Miscanthus grasses in Taiwan and Thailand (Acari, Tetranychidae). Syst Appl Acarol 24:675–682

    Google Scholar 

  • Sato Y (2004). Studies on variation in social structure and the maintenance mechanism associated with diversification in the Stigmaeopsis species group. In: Hokkaido University, Ph. D. thesis,, p 162

  • Sato Y, Breeuwer JAJ, Egas M, Sabelis MW (2015) Incomplete premating and postmating reproductive barriers between two parapatric populations of a social spider mite. Exp Appl Acarol 65:277–291

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Egas M, Sabelis MW, Mochizuki A (2013a) Male–male aggression peaks at intermediate relatedness in a social spider mite. Ecol Evol 3:2661–2669

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Sabelis MW, Mochizuki A (2013b) Asymmetry in male lethal fight between parapatric forms of a social spider mite. Exp Appl Acarol 60:451–461

    Article  PubMed  Google Scholar 

  • Sato Y, Saito Y (2007) Can the extremely female-biased sex ratio of the social spider mites be explained by Hamilton’s local mate competition model? Ecol Entomol 32:597–602

    Article  Google Scholar 

  • Sato Y, Saito Y, Chittenden AR (2008) The parapatric distribution and contact zone of two forms showing different male-to-male aggressiveness in a social spider mite, Stigmaeopsis miscanthi (Acari: Tetranychidae). Exp Appl Acarol 44:265–276

    Article  PubMed  Google Scholar 

  • Sato Y, Saito Y, Mori K (2000a) Reproductive isolation between populations showing different aggression in a subsocial spider mite, Schizotetranychus miscanthi Saito (Acari: Tetranychidae). Appl Entomol Zool 35:605–610

    Article  Google Scholar 

  • Sato Y, Saito Y, Mori K (2000b) Patterns of reproductive isolation between two groups of Schizotetranychus miscanthi Saito (Acari: Tetranychidae) showing different male aggression traits. Appl Entomol Zool 35:611–618

    Article  Google Scholar 

  • Sato Y, Sakamoto H, Gotoh T, Saito Y, Chao J-T, Egas M et al. (2018) Patterns of reproductive isolation in a haplodiploid – strong postmating, prezygotic barriers among three forms of a social spider mite. J Evolut Biol 31:866–881

    Article  CAS  Google Scholar 

  • Sato Y, Tsuda Y, Sakamoto H, Egas M, Gotoh T, Saito Y et al. (2019) Phylogeography of lethal male fighting in a social spider mite. Ecol Evolut 9:1590–1602

    Article  Google Scholar 

  • Schausberger P, Yano S, Sato Y (2021) Cooperative behaviors in group-Living spider mites. Front Ecol Evolut 9:745036

    Article  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evolut 19:198–207

    Article  Google Scholar 

  • Smadja C, Butlin R (2006) Speciation: A new role for reinforcement. Heredity 96:422–423

    Article  CAS  PubMed  Google Scholar 

  • Suetsugu K, Hirota SK, Shitara T, Ishida K, Nakato N, Hayakawa H et al. (2023) The absence of bumblebees on an oceanic island blurs the species boundary of two closely related orchids. N. Phytologist 241:1321–1333

    Article  Google Scholar 

  • Suyama Y, Hirota SK, Matsuo A, Tsunamoto Y, Mitsuyuki C, Shimura A et al. (2022) Complementary combination of multiplex high-throughput DNA sequencing for molecular phylogeny. Ecol Res 37:171–181

    Article  CAS  Google Scholar 

  • Suyama Y, Matsuki Y (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci Rep. 5:16963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Venables WN, Ripley BD (2002) Modern Applied Statistics with S, 4th edn. Springer-Verlag: New York

  • West SA (2010) Sex Allocation. Princeton Univ Press

  • Wood ZT, Wiegardt AK, Barton KL, Clark JD, Homola JJ, Olsen BJ, King BL, Kovach AI, Kovach MT (2021) Meta‐analysis: Congruence of genomic and phenotypic differentiation across diverse natural study systems. Evolut Appl 14:2189–2205

    Article  Google Scholar 

  • Yano J, Saito Y, Chittenden AR, Sato Y (2011) Variation in counterattack effect against a phytoseiid predator between two forms of the social spider mite, Stigmaeopsis miscanthi. J Ethol 29:337–342

    Article  Google Scholar 

Download references

Acknowledgements

We thank Dr. Kentaro Nakano, Dr. Yooichi Kainoh and Tsukuba Experimental Forest, Mountain Science Center at the University of Tsukuba for providing the microscope for male morphology measurements and the space to cultivate the host plants of the mites. We thank Dr. Kyoichi Sawamura, Dr. Tomoki Chiba, Mr. Gomei Yoda, Ms. Hisaho Kobatyashi, Mr. Taito Sano, Mr. Ryuto Uchiyama, Ms. Sayuka (Nagase) Nitta, Ms. Aina Yokoi, and Ms. Ayana Tanino for their valuable suggestions and support. This research was supported in part by JSPS KAKENHI, Grant Number 20K06810 (Grant-in-Aid for Scientific Research C to Y. Sato), by JSPS KAKENHI, Grant Number 24H00055 (Grant-in-Aid for Scientific Research S to Y.T), by The Research Enhancement Project of Mountain Science Center, University of Tsukuba (to Y.Sato), by Nakatsuji Foresight Foundation (to Y.Sato), and by The Suzuki Takahisa Memorial Grant, University of Tsukuba (to Y. Sato).

Author information

Author notes

  1. These authors contributed equally: Shota Konaka, Shun K. Hirota, Yukie Sato.

Authors and Affiliations

  1. Master Program in Biology, Degree Programs in Life and Earth Sciences, Graduate School of Science and Technology, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8572, Japan

    Shota Konaka & Naoki Matsumoto

  2. Field Science Center, Graduate School of Agricultural Science, Tohoku University, 232-3 Yomogida, Naruko-onsen, Osaki, Miyagi, 989-6711, Japan

    Shun K. Hirota & Yoshihisa Suyama

  3. Botanical Gardens, Osaka Metropolitan University 2000 Kisaichi, Katano City, Osaka, 576-0004, Japan

    Shun K. Hirota

  4. Faculty of Life and Environmental Sciences / Mountain Science Center, University of Tsukuba, 1-1-1 Tennodai, Tsukuba, Ibaraki, 305-8577, Japan

    Yukie Sato & Yoshihiko Tsumura

Authors
  1. Shota Konaka
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shun K. Hirota
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yukie Sato
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Naoki Matsumoto
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yoshihisa Suyama
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yoshihiko Tsumura
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Y. Sato conceived the study. Y. Sato, S. Konaka, Y. Tsumura, and Y. Suyama designed the study. S. Konaka, Y. Sato, and N. Matsumoto conducted the field surveys. S. Konaka performed the measurements, Y. Sato and S. Konaka analysed male morphology. S. Hirota, Y. Suyama, S. Konaka, Y. Sato, and Y. Tsumura performed molecular analyses. Y. Sato conducted the cross-experiment and analysed reproductive isolation. Y. Sato and S. Hirota wrote the first draft of the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Yukie Sato.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Associate editor: Ben Evans.

Supplementary information

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Konaka, S., Hirota, S.K., Sato, Y. et al. Secondary contact zone and genetic introgression in closely related haplodiploid social spider mites. Heredity (2024). https://doi.org/10.1038/s41437-024-00708-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41437-024-00708-y

Search

Advanced search

Quick links