Quantitative Ecological Genetics of Biotic Interaction

We are interested in how genetic variation shapes, and is shaped by, biotic interactions. To analyze quantitative genetic variation in complex ecological traits, our research employs cutting-edge tools of computational biology and functional genomics. Currently, we are working on plants and insects, but other projects involving biotic interactions are also welcome.
Keywords: Plant Ecology, Quantitative Genetics, Biotic Interaction

1. Quantitative Genetics of Plant-Plant Interaction

Plants cannot escape from neighboring individuals in the field, making plant-plant interactions unavoidable in a local space. Despite the prevalence of neighboring plant-plant interactions, these interactions are not always attributable to a single trait or gene. To dissect the genetic architecture of intraspecific plant-plant interactions, we developed new methods named “Neighbor GWAS” (Sato et al. 2021 Heredity) and “Neighbor QTL” (Sato et al. 2021 G3). These methods are being applied to the analysis of insect herbivory and communities on Arabidopsis thaliana accessions (Sato et al. 2024 Nature Communications) in addition to other quantitative traits in crops, trees, etc… We are also seeking the potential application of intraspecific plant-plant interactions to improve plant resistance and yield by mixed planting.

Field experiment using Arabidopsis thaliana accessions. Modified from Sato et al. (2021) Heredity

2. Evolutionary Ecology of Plant Defense Against Herbivores

Plants develop various defense traits against herbivores. Such anti-herbivore defense traits exhibit polymorphisms within a natural plant population, which leads us to ask how these polymorphisms can be maintained in nature. By focusing on neighboring plants, we found that hairy plants were less damaged by a leaf beetle when surrounded by glabrous plants in the wild herb Arabidopsis halleri. Such neighbor effects further exerted negative frequency-dependent selection on GLABRA1-based trichome dimorphism (Sato & Kudoh 2017 American Naturalist; Sato et al. 2017 Functional Ecology). These findings highlight the importance of neighbor effects in the maintenance of genetic variation in anti-herbivore defense traits (reviewed in Sato 2018 Plant Species Biology).

Hairy Arabidopsis halleri (left) and larval Phaedon brassicae (right) from Plant Species Biology Vol. 33(2)

Principal Investigator

Yasuhiro Sato (Assistant Professor)

My research career began at Kyoto University in Japan. After obtaining my PhD in 2016, I experienced two postdoc positions in Japan and a senior postdoc position in Switzerland. Since 2024, I have been appointed as a tenure-track assistant professor at Hokkaido University. My research interests include ecological genetics of biotic interactions involving plants. See also CV for the full profile.
ORCID: 0000-0002-6466-723X; ResearcherID: N-7939-2013

Postdocs

Currently none

PhD students

• Iqra Akram (EXEX Doctoral fellow)
  After obtaining MSc in agriculture, Iqra has been working on the genetics of plant-plant interactions in crop species since 2024.

Master students

Currently none

Support staff

• Miho Kawagoe (Administrative assistant)

Preprint

Currently none

Peer-reviewed articles

1. Sato Y*, Shimizu-Inatsugi R, Takeda K, Schmid B, Nagano AJ*, Shimizu KK*. (2024) Reducing herbivory in mixed planting by genomic prediction of neighbor effects in the field. Nature Communications 15:8467. https://doi.org/10.1038/s41467-024-52374-7 [Media release at University of Zurich; EN, DE]

2. Stockenhuber R, Akiyama R, Tissot N, Milosavljevic S, Yamazaki M, Wyler M, Arongaus AB, Podolec R, Sato Y, Widmer A, Ulm R*, Shimizu KK*. (2024) UV RESISTANCE LOCUS 8-mediated UV-B response is required alongside CRYPTOCHROME 1 for plant survival in sunlight under field conditions. Plant and Cell Physiology 65:35-48. https://doi.org/10.1093/pcp/pcad113

3. The Herbivory Variability Network. (2023) Plant size, latitude, and phylogeny explain variability in herbivory. Science 382:679-683. https://doi.org/10.1126/science.adh8830 [a consortium paper incl. Y. Sato as one of the co-authors]

4. Xu C^†, Sato Y^†*, Yamazaki M, Brasser M, Barbour MA, Bascompte J, Shimizu KK*. (2023) Genome-wide association study of aphid abundance highlights a locus affecting plant growth and flowering in Arabidopsis thaliana. Royal Society Open Science 10:230399. https://doi.org/10.1098/rsos.230399

5. Sato Y*, Takahashi Y, Xu C, Shimizu KK*. (2023) Detecting frequency-dependent selection through the effects of genotype similarity on fitness components. Evolution 77:1145–1157. https://doi.org/10.1093/evolut/qpad028 [Vignette]

6. Shimizu-Inatsugi R*, Morishima A, Mourato B, Shimizu KK, Sato Y. (2023) Phenotypic variation of a new synthetic allotetraploid Arabidopsis kamchatica enhanced in natural environment. Frontiers in Plant Science 13:1058522 https://doi.org/10.3389/fpls.2022.1058522

7. Takimoto H^†*, Sato Y^†, Nagano AJ, Shimizu KK, Kanagawa A. (2021) Using a two-stage convolutional neural network to rapidly identify tiny herbivorous beetles in the field. Ecological Informatics 66:101466 https://doi.org/10.1016/j.ecoinf.2021.101466

8. Sato Y, Yamamoto E, Shimizu KK*, Nagano AJ*. (2021) Neighbor GWAS: incorporating neighbor genotypic identity into genome-wide association studies of field herbivory. Heredity 126(4):597–614. https://doi.org/10.1038/s41437-020-00401-w [R package]

9. Sato Y^†*, Takeda K^†, Nagano AJ*. (2021) Neighbor QTL: an interval mapping method for quantitative trait loci underlying plant neighborhood effects. G3; Genes|Genomes|Genetics 11(2):jkab017. https://doi.org/10.1093/g3journal/jkab017 [R package]

10. Shimizu-Inatsugi R*, Milosavljevic S, Shimizu KK, Schaepman-Strub G, Tanoi K, Sato Y. (2021) Metal accumulation and its effect on leaf herbivory in an allopolyploid species Arabidopsis kamchatica inherited from a diploid hyperaccumulator A. halleri. Plant Species Biology 36(2):208–217. https://doi.org/10.1111/1442-1984.12304

11. Sato Y, Tezuka A, Kashima M, Deguchi A, Shimizu-Inatsugi R, Yamazaki M, Shimizu KK*, Nagano AJ*. (2019) Transcriptional variation in glucosinolate biosynthetic genes and inducible responses to aphid herbivory on field-grown Arabidopsis thaliana. Frontiers in Genetics 10:787. https://doi.org/10.3389/fgene.2019.00787

12. Sato Y, Shimizu-Inatsugi R, Yamazaki M, Shimizu KK*, Nagano AJ*. (2019) Plant trichomes and a single gene GLABRA1 contribute to insect community composition on field-grown Arabidopsis thaliana. BMC Plant Biology 19:163. https://doi.org/10.1186/s12870-019-1705-2

13. Nakadai R^†*, Hashimoto K^†, Iwasaki T, Sato Y. (2018) Geographical co-occurrence of butterfly species: the importance of niche filtering by host plant species. Oecologia 186(4):995–1005. https://doi.org/10.1007/s00442-018-4062-1

14. Sato Y^†*, Ito K^†, Kudoh H. (2017) Optimal foraging by herbivores maintains polymorphism in defence in a natural plant population. Functional Ecology 31(12):2233-2243. https://doi.org/10.1111/1365-2435.12937 [postprint]

15. Sato Y*, Kudoh H. (2017) Herbivore-mediated interaction promotes the maintenance of trichome dimorphism through negative frequency-dependent selection. The American Naturalist 190(3):E67-E77. https://doi.org/10.1086/692603 [PDF]

16. Sato Y*, Kudoh H. (2017) Fine-scale frequency differentiation along a herbivory gradient in the trichome dimorphism of a wild Arabidopsis. Ecology and Evolution 7(7):2133-2141. https://doi.org/10.1002/ece3.2830

17. Sato Y*, Kudoh H. (2016) Presence of substitute diets alters plant resistance to specialist and generalist herbivores: a meta-analysis. Ecosphere 7(11):e01446 https://doi.org/10.1002/ecs2.1446

18. Sato Y*, Kudoh H. (2016) Associational effects against a leaf beetle mediate a minority advantage in defense and growth between hairy and glabrous plants. Evolutionary Ecology 30(1):137-154. https://doi.org/10.1007/s10682-015-9809-0 [postprint]

19. Sato Y*, Sato S. (2015) Spring temperature predicts the long-term molting phenology of two cicadas, Cryptotympana facialis and Graptopsaltria nigrofuscata (Hemiptera: Cicadidae). Annals of the Entomological Society of America 108(4):494-500. https://doi.org/10.1093/aesa/sav036 [postprint]

20. Sato Y*, Kudoh H. (2015) Tests of associational defence provided by hairy plants for glabrous plants of Arabidopsis halleri subsp. gemmifera against insect herbivores. Ecological Entomology 40(3):269-279. https://doi.org/10.1111/een.12179 [postprint]

21. Sato Y, Kudoh H*. (2014) Fine-scale genetic differentiation of a temperate herb: relevance of local environments and demographic change. AoB PLANTS 6:plu070. https://doi.org/10.1093/aobpla/plu070

22. Sato Y*, Kawagoe T, Sawada Y, Hirai MY, Kudoh H. (2014) Frequency-dependent herbivory by a leaf beetle, Phaedon brassicae, on hairy and glabrous plants of Arabidopsis halleri subsp. gemmifera. Evolutionary Ecology 28(3):545-559. https://doi.org/10.1007/s10682-013-9686-3 [postprint]

23. Sato Y*, Kudoh H. (2013) Relative strength of phenotypic selection on the height and number of flowering-stalks in the rosette annual Cardamine hirsuta (Brassicaceae). Journal of Ecology and Environment 36(3):151-158. https://doi.org/10.5141/ecoenv.2013.151

24. Sato Y*, Takakura KI, Nishida S, Nishida T. (2013) Dominant occurrence of cleistogamous flowers of Lamium amplexicaule in relation to the nearby presence of an alien congener L. purpureum. ISRN Ecology Article ID:476862. http://dx.doi.org/10.1155/2013/476862

Peer-reviewed monographs/reviews

1. Sato Y*, Wuest SE*. (2024) The genetics of plant–plant interactions and their cascading effects on agroecosystems – from model plants to applications. Plant and Cell Physiology https://doi.org/10.1093/pcp/pcae092

2. Sato Y*. (2018) Associational effects and the maintenance of polymorphism in plant defense against herbivores: review and evidence. Plant Species Biology 33(2):91-108. https://doi.org/10.1111/1442-1984.12201 [postprint]

3. Sakata Y*, Sato Y. (2017) Evolutionary ecology of plant defense: integrating different spatial scales within and among species (in Japanese). Japanese Journal of Ecology 67(3):287-306. https://doi.org/10.18960/seitai.67.3_287

Peer-reviewed conference proceedings

1. Kuzuhara H, Takimoto H, Sato Y, Kanagawa A. (2020) Insect pest detection and identification method based on deep learning for realizing a pest control system. Proceedings of the Society of Instrument and Control Engineers (SICE) Annual Conference 2020. pp. 709–714. https://doi.org/10.23919/SICE48898.2020.9240458

Books/Book chapters

1. Sato Y. (2024) Chapter 7: The maintenance of trichome dimorphism through associational effects: a case study of Arabidopsis halleri and a leaf beetle (in Japanese). In: Ecology of Plant Defense Against Herbivores (Y. Sakata and T. Tsunoda eds), Species Biology Series, Bun-ichi Sogo Shuppan, Tokyo, Japan. ISBN: 978-4-8299-6211-4.

2. Sato Y, Muranaka T. (eds). (2023) Trans-Scale Biology of Plants: Integrating genomics, phenomics, and ecology to unveil biodiversity (in Japanese). Species Biology Series, Bun-ichi Sogo Shuppan, Tokyo, Japan. ISBN: 978-4-8299-6210-7.