Species complex diversification by host plant use in an herbivorous insect: The source of Puerto Rican cactus mealybug pest and implications for biological control

Authors: POVEDA-MARTINEZ, DANIEL - Fuedei; AGUIRRE, MARIA - Fuedei; Hight, Stephen; TRIAPITSYN, SERGUEI - University Of California; DIAZ-SOLTERO, HILDA - Animal And Plant Health Inspection Service (APHIS); VITORINO, MARCELO - Universidade Regional De Blumenau(FURB); HASSON, ESTEBAN - Universidad De Buenos Aires

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/29/2020
Publication Date: 8/20/2020
Citation: Poveda-Martinez, D., Aguirre, M.B., Hight, S.D., Triapitsyn, S.V., Diaz-Soltero, H., Vitorino, M.D., Hasson, E. 2020. Species complex diversification by host plant use in an herbivorous insect: The source of Puerto Rican cactus mealybug pest and implications for biological control. Ecology and Evolution. 00:1-18. https://doi.org/10.1002/ece3.6702.
DOI: https://doi.org/10.1002/ece3.6702

Interpretive Summary: The Harrisia cactus mealybug (HCM) was introduced into Puerto Rico around 2000 and was found destroying several native cactus species in the dry forest habitat of Puerto Rico. The HCM has also invaded Florida (feeding on amaranth plants) and California (feeding on cactus), causing concerns for the safety of native cactus in North America. To identify the source of the pest cactus-feeding mealybugs, HCM collected from various host plants at differing locations around the world were characterized using genetic identification by scientists with USDA, Agricultural Research Service, Center for Medical, Agricultural and Veterinary Entomology, Tallahassee, Florida, in collaboration with USDA-APHIS, the Argentine Foundation for the Study of Invasive Species, and Universities of California and Argentina. The original HCM species group was found to be comprised of five different species of mealybugs with each species feeding on specific host plants. The mealybugs feeding on species of amaranth and purslane plants in Puerto Rico and Florida originated from northeastern Brazil and were a non-pest invasive species. The mealybugs infesting cactus in Puerto Rico were an invasive species from southeastern Brazil and were genetically identical to cactus-feeding mealybugs in California. Fortunately, the California pest mealybug population was eradicated by state authorities, but a concern exists that additional introductions will be made. Knowing the geographic origin of the Puerto Rican mealybug focuses the need to search for natural enemies as biological control agents from southeastern Brazil before another invasive introduction occurs.

Technical Abstract: Cryptic taxa have often been observed in the form of host-associated species that diverged as the result of adaptation to alternate host plants. Untangling cryptic diversity in species complexes that encompass invasive species is a mandatory task for pest management. Moreover, investigating the evolutionary history of a species complex may help to understand the drivers of their diversification. The mealybug Hypogeococcus pungens was believed to be a polyphagous species from South America and has been reported as a pest devastating native cacti in Puerto Rico, also threatening cactus diversity in the Caribbean and North America. There is neither certainty about the identity of the pest, nor the source population from South America. Recent studies pointed to substantial genetic differentiation among local populations, suggesting that H. pungens is a species complex. In this study, we used a combination of genome-wide SNPs and mtDNA variation to investigate species diversity within H. pungens sensu lato to establish host plant ranges of each one of the putative members of the complex, to evaluate whether the pattern of host plant association drove diversification in the species complex, and to determine the source population of the Puerto Rican cactus pest. Our results suggested that H. pungens comprises at least five different species, each one strongly associated with specific host plants. We also established that the Puerto Rican cactus pest derives from southeastern Brazilian mealybugs. This is an important achievement because it will help to design reliable strategies for biological control using natural enemies of the pest from its native range.