Genetic population structure and reproductive system of two invasive Asian earthworms, Amynthas tokioensis and Amynthas agrestis

Maryam Nouri-Aiin; Samantha Connolly; Cheryl Keough; Annie Jean Smigelsky; Yiyi Wen; Jeremy Howland; Jos J Schall; Josef H Görres

doi:10.7717/peerj.13622

Genetic population structure and reproductive system of two invasive Asian earthworms, Amynthas tokioensis and Amynthas agrestis

PeerJ. 2022 Jul 13:10:e13622. doi: 10.7717/peerj.13622. eCollection 2022.

Authors

Maryam Nouri-Aiin¹, Samantha Connolly², Cheryl Keough¹, Annie Jean Smigelsky¹, Yiyi Wen³, Jeremy Howland¹, Jos J Schall⁴, Josef H Görres¹

Affiliations

¹ Plant and Soil Science Department, University of Vermont, Burlington, VT, United States of America.
² Plant Biology Department, University of Vermont, Burlington, VT, United States of America.
³ Environmental Science, Rubinstein School of the Environment, University of Vermont, Burlington, VT, United States of America.
⁴ Department of Biology, University of Vermont, Burlington, VT, United States of America.

Abstract

The invasive Asian earthworms, Amynthas tokioensis and A. agrestis, have been successful in entering North American forests in recent decades, with significant damage to both soils and above-ground environments. This success could be driven in part by a polyploid genetic system and parthenogenetic reproduction, often suggested as benefits for invasive species. Therefore, we assessed the genetic population structure, genetic diversity, and reproductive system of both species using morphological traits and panels of microsatellite markers. A total of 216 A. tokioensis and 196 A. agrestis from six sites in Vermont USA were analyzed. Although all worms were morphologically hermaphroditic, all the A. agrestis lacked the male pore (the structure allowing pass of sperm between individuals), and only 19% of the A. tokioensis possessed the male pore. All A. tokioensis earthworms were triploid (scored for three alleles for at least 1 locus, and usually several), and A. agrestis was a mix of triploid and diploid individuals. Notable was the high proportion (80%) of A. agrestis earthworms that were diploid at one site. There was clearly clonal reproduction, with identical seven- locus genotypes observed for earthworms from each site, with as many as 45 individuals with the identical genotype at one site. However, the earthworms were also genetically diverse, with 14 genotypes observed for A. tokioensis and 54 for A. agrestis, and with many singleton genotypes (a single individual). Most genotypes (71% for A. tokioensis and 92% for A. agrestis) were found at a single site. The greatest number of genotypes was found at a commercial nursery where fully 23/26 A. agrestis earthworms were singleton genotypes. As expected for the pattern of private clone alleles at sites, several measures of geographic genetic differentiation were positive, and as expected for triploid systems, an AMOVA analysis showed high within-individual genetic diversity. The paradox of clear clonal reproduction, but with a great number of genotypes for each species, and the mix of triploid and diploid individuals could be explained if the worms have been sexually reproductive, with the switch to the uniparental system only recently (or even if sexual reproduction is episodic). Last, a large number of microsatellite loci were recovered for each species and there sequence and suggested PCR primers are provided for free use by other researchers.

Keywords: Amynthas; Clonality; Genetic diversity; Invasive earthworms; Jumping worms; Micorsatellite markers; Ploidy level; Population genetic structure; Reproductive system.

Publication types

Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

Animals
Genetic Structures
Genitalia
Male
Oligochaeta* / genetics
Semen
Triploidy

Grants and funding

This work was supported by USDA National Institute of Food and Agriculture (Hatch project 1018366) and two anonymous donors who contributed directly to the University of Vermont in support of this research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.