Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control

Authors: STAHLKE, AMANDA - University Of Idaho; BITUME, ELLYN - Us Forest Service (FS); OZSOY, ZEYNEP - Colorado Mesa University; BEAN, DAN - Colorado Department Of Agriculture; VEILLET, ANNE - University Of Idaho; CLARK, MEGHAN - Michigan State University; CLARK, ELIZA - Colorado State University; Moran, Patrick; HUFBAUER, RUTH - Colorado State University; HOHENLOHE, PAUL - University Of Idaho

Submitted to: Evolutionary Applications
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 11/8/2021
Publication Date: 1/1/2022
Citation: Stahlke, A.R., Bitume, E., Ozsoy, Z.A., Bean, D.W., Veillet, A., Clark, M., Clark, E., Moran, P.J., Hufbauer, R., Hohenlohe, P.A. 2022. Hybridization and range expansion in tamarisk beetles (Diorhabda spp.) introduced to North America for classical biological control. Evolutionary Applications. 15(1):60-77. https://doi.org/10.1111/eva.13325.
DOI: https://doi.org/10.1111/eva.13325

Interpretive Summary: Invasive, non-native weeds of wild wetlands, shoreline, forest, rangeland and desert habitats are difficult or impossible to control using conventional methods such as herbicides or mechanical removal. In many cases, insects from the native range of the weed can be found that are safe (they only feed on the weed and not on native natural plants or crops) and effective (they do a lot of damage to the weed, causing death, reduced growth, reduced reproduction, and/or reduced spread). The shrub or small tree known as tamarisk or saltcedar, consisting of several species in the genus Tamarix and their natural hybrids, is one of the most widespread and damaging invasive plants in the arid western U.S., particularly along the shorelnes of rivers, reservoirs, creeks and arroyos. To help control this invasive plant, the USDA-ARS discovered and released four species of leaf-feeding beetles, collected originally from different parts of the native range of tamarisk, including one from northern China and Kazakhstan, one from Uzbekistan,one from mainland Greece and the island of Crete (Greece), and one from Tunisia. The four species were released to try to establish the beetles for biological control of tamarisk across the wide invaded range in the U.S., from Montana to southwestern Texas and westward to California. In this study, beetles were collected from the original source locations in the native range or from original lab-reared colonies from those collections, and were compared using DNA fingerprinting to field populations at the site of first release in the U.S., at other sites to which each beetle species dispersed, and in areas where the beetle species overlapped and, contrary to original expectations, mated with each other and produced hybrids. It was found that, as expected, the genetic diversity of the original U.S.-released populations was low compared to the source populations in the native range of tamarisk, indicating that a genetic 'bottleneck' occurred in transporting and rearing the beetles. However, diversity increased substantially as the beetle species spread in the western U.S., especially when two, three, or even all four species overlapped in their dispersal areas,particularly in New Mexico and Texas. One species, known as the northern tamarisk beetle (Diorhabda carinulata), spread (with help from humans in some cases) from original release locations in Wyoming (sourced from Fukang, China) and Utah (sourced from Chilik, Kazakhstan) into Colorado, Nevada, Arizona, New Mexico, and Texas, and genetic diversity increased as the Chinese and Kazakhstan populations mixed, with the Kazakhstan population dominating field populations. Two other species-the larger tamarisk beetle from Uzbekistan (Diorhabda carinata) released originally in northwestern Texas; and the subtropical tamarisk beetle from Tunisia (Diorhabda sublineata), released originally along the Rio Grande in southwestern Texas-hybridized most frequently, among all populations of all four beetle species sampled, as they were found at 24 of about 40 sites sampled. These hybrids dominated beetle populations in Texas and New Mexico, while only the parental Uzbekistan beetle line was found in Oklahoma and Kansas. One tri-species hybrid was found (D. carinulata x D. carinata x D. sublineata). The results demonstrate how the tamarisk beetles have spread and interacted across the western U.S. The results may also help in interpreting the cause of variable success of the beetles to control tamarisk in the western U.S.

Technical Abstract: As a planned invasion, classical biological control (biocontrol) agents present important opportunities to identify the mechanisms of establishment and spread in a novel environment. In some biocontrol systems, multiple source populations (ecotypes) or congeneric species are released to increase the chance of ecological matching across diverse habitat of the invasive species; or, the presence of cryptic species becomes apparent after release. Undoubtedly, eco-evolutionary forces will interact to shape the outcomes of introduction and secondary contact among biocontrol agents; yet the genomic consequences of founder effects and gene flow have rarely been studied. Here we examine the genome-wide outcomes of introduction, spread, and gene flow in four cryptic species of a biocontrol agent, the tamarisk beetle (Diorhabda carinata, D. carinulata, D. elongata, and D. sublineata), introduced from six localities across Eurasia to control the invasive shrub tamarisk (Tamarix spp.) in western North America. We assembled a de novo draft genome and used reference-based RADseq for over 500 individuals from laboratory cultures, the native range, and across the introduced range to characterize the genetic variation associated with establishment, spread, and gene flow. We found differential establishment and spread among the six released populations. Despite evidence of a substantial genetic bottleneck among collections of D. carinulata in North America and low levels of genetic diversity, populations continue to establish and spread, with one D. carinulata ecotype dominating the southward expansion front.¬ We confirmed that D. carinata, D. elongata, and D. sublineata hybridize in the field to varying extents, although D. carinata x D. sublineata hybrids were the most abundant and indicated a lack of reproductive barriers. Genetic diversity was greater among populations with hybrids, highlighting potential for increased adaptive potential due to gene flow. Our results provide a molecular snapshot of field dynamics and the foundation for further application of genomics to understand contemporary eco-evolution in classical biological control programs.