4.7 Article

Human-mediated eco-evolutionary processes of the herbivorous insect Hyalopterus arundiniformis during the Holocene

Journal

DIVERSITY AND DISTRIBUTIONS
Volume 28, Issue 6, Pages 1313-1326

Publisher

WILEY
DOI: 10.1111/ddi.13541

Keywords

anthropogenic activity; cryptic invasion; herbivorous insect; Holocene; human niche construction; migratory episodes; silk road

Funding

  1. Key Collaborative Research Program of the Alliance of International Science Organizations [ANSO-CR-KP-2020-04]
  2. National Natural Science Foundation of China [31750002, 31772492, 32030014]
  3. Second Tibetan Plateau Scientific Expedition and Research (STEP) program [2019QZKK05010601]
  4. Youth Innovation Promotion Association of the Chinese Academy of Sciences [2020087]

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This study investigates the impact of human activity during the Holocene on the evolutionary trajectory of insect pests. By integrating archaeological evidence, phylogeographic analyses, and a climatic niche-based approach, the researchers study the dispersal and demographic dynamics of Hyalopterus arundiniformis (HAR) using peach as its host plant. The study reveals that human-mediated dispersal of the host plant during the Holocene resulted in the expansion of HAR's geographic range, effective population size, and climatic niche breadth.
Aim Pleistocene climatic fluctuations have been identified as a dominant factor in evolutionary and ecological processes underlying contemporary species distribution. In contrast, anthropogenic activity during the Holocene has been largely neglected in phylogeographic inference. Here, by integrating archaeological evidence, phylogeographic analyses and a climatic niche-based approach, the role of Holocene human activity in determining the evolutionary trajectory of insect pests is investigated using Hyalopterus arundiniformis (HAR) as a model. Location Eurasia. Methods We compiled archaeological records and historical data for the host plant (i.e. peach) of HAR. Phylogeographic structure, genetic diversity and gene flow were estimated. Historical demographic dynamics were explored using coalescent-based analyses. The origin and dispersal history were assessed using an approximate Bayesian computation (ABC) approach. The changes in climatic niche breadth during geographic expansion were evaluated via niche comparison analyses. Results Our results revealed that HAR originated in Southwest China and dispersed to Southeast and Northwest China, and it was then introduced to western Eurasia from Northwest China. The climatic niche shifted significantly with range expansions, and niche expansion explained the largest proportion of niche dynamics. Population size expansion occurred in the Holocene and coincided with the domestication and trans-Eurasian trade of peach. Main conclusions The geographic range, effective population size and climatic niche breadth of HAR expanded following the human-mediated dispersal of its host plant during the Holocene. Our results highlight that the expansion of Neolithic agriculture and trans-Eurasian crop exchange along ancient communication routes may have played an important role in shaping the distribution and demographic dynamics of herbivorous insects. This study also provides essential information for pest management and biological invasions.

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