Untangling the Hypogeococcus pungens species complex (Hemiptera: Pseudococcidae) for Argentina, Australia, and Puerto Rico based on host plant associations and genetic evidence

Authors: POVEDA-MARTINEZ, DANIEL - Fuedei; AGYURREM, NARUA - Fuedei; LOGARZO, GUILLERMO - Fuedei; CALDERON, L - Consejo Nacional De Investigaciones Científicas Y Técnicas(CONICET); DE LA COLINA, A - Universidad De Buenos Aires; Hight, Stephen; TRIAPITSYN, SERGUEI - University Of California; DIAZ-SOLTERO, HILDA - Animal And Plant Health Inspection Service (APHIS); HASSON, ESTEBAN - Universidad De Buenos Aires

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/18/2019
Publication Date: 7/25/2019
Citation: Poveda-Martinez, D., Agyurrem, N.B., Logarzo, G.A., Calderon, L., De La Colina, A., Hight, S.D., Triapitsyn, S.V., Diaz-Soltero, H., Hasson, E. 2019. Untangling the Hypogeococcus pungens species complex (Hemiptera: Pseudococcidae) for Argentina, Australia, and Puerto Rico based on host plant associations and genetic evidence. PLoS One. 14(7):e0220366. https://doi.org/10.1371/journal.pone.0220366.
DOI: https://doi.org/10.1371/journal.pone.0220366

Interpretive Summary: A species of mealybug native to South America, commonly known as the Harrisia cactus mealybug (HCM), was introduced into Puerto Rico where it is attacking and destroying several species of native Puerto Rican cactus. However, the taxonomic identity of this insect is in question because it not only feeds on species of cactus, but also on plants in the amaranth and portulaca families. 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 used genetic markers to determine that the “Harrisia cactus mealybug” is a complex of at least three mealybug species. Use of these markers in additional molecular genetic analysis of mealybug populations in Brazil, Argentina, Paraguay, and Florida may identify the geographic origin of the Puerto Rican mealybug pest, targeting the search for natural enemies to be used in biological control programs against this pest. Also, since the species of HCM found on non-cactus host plants is a different species than the HCM found on cactus, there is little risk of the non-cactus HCM species found in Florida moving onto susceptible cactus host plants.

Technical Abstract: Hypogeococcus pungens, a mealybug native of southern South America, is devastating native cacti in Puerto Rico and threatening cactus diversity in the Caribbean, and potentially in Central and North America. The taxonomic status of H. pungens is controversial since it has been reported feeding not only on Cactaceae but also on Amaranthaceae throughout its distribution range. However, in Australia, where the species had been exported from Argentina to control weedy American cacti, it was never found on host plants other than Cactaceae. These conflicting pieces of evidence not only cast doubt on the species identity that invaded Puerto Rico, but also have a negative impact on the search for natural enemies to be used in biological control programs against this pest. Here, we present genetic evidence suggesting that H. pungens is a species complex driven by their host plants. The nuclear EF1a and 18S and the mitochondrial COI genes were used as markers to evaluate the phylogenetic relationships among H. pungens populations collected in Argentina, Australia and Puerto Rico feeding on Cactaceae and/or Amaranthaceae. Species delimitation analyses were conducted based on single and multi-locus approaches combined with phylogenetic analyses. Two well-supported species were found, H. pungens included mealybugs feeding on Amaranthaceae and a new undescribed Hypogeococcus species using Cactaceae as hosts. Moreover, the Bayesian method also indicated that the Australian mealybug population derives from a new undescribed species. The genetic differentiation between the members of the complex may be interpreted as the result of recent speciation events prompted by host plant shifts. Finally, the finding of a single haplotype in the Puerto Rico population suggests only one invasive event, however, we could not identify the geographic origin of the pest, a necessary task to implement effective plans for biological control to reduce the threat to the diversity of cacti in the Caribbean.