4.2 Puerto Rican cactus mealybugs derive from southeastern Brazilian cactus feeding populations
Our analyses, based on nuclear SNPs and mtDNA, allowed us to establish that the Puerto Rican cactus pest derives from a population similar to the southeastern Brazilian cactus feeding clade (Figure 2 and 3). In our previous study using only mtDNA and restricted sampling in the native range (Argentina), the Puerto Rican cactus pest clustered close toH. pungens sensu stricto (Poveda-Martínez et al., 2019). However, when we expanded the sampling to Paraguay and along the southeast and northeastern Atlantic coast of Brazil and extended the genetic sampling to genome-wide SNPs, we found that the Puerto Rican cactus pest fell into the same clade with populations from southeastern Brazil (Figure 2). Moreover, samples collected on Cactaceae in southern California shared the same and unique mtDNA haplotype with the Puerto Rican cactus pest. This finding is a warning of the threat that the presence of this pest represents to cactus diversity in the United States and Mexico, where cactus diversity is high. Since the first detection of the pest in Puerto Rico in 2005 (Segarra-Carmona et al., 2010), the mealybug now attacks half of the 14 native Puerto Rican cactus species (including three endemic and two endangered species) occurring in dry forests, causing large gall-like tissue deformations that often lead to high plant mortality (Carrera-Martínez et al., 2015; Triapitsyn et al., 2020). With the new record of the pest in California, the pest has spread beyond its current distribution range to potential cactus hosts throughout North America (including Mexico) and the Caribbean. Identification of the source of the cactus pest that invaded Puerto Rico and the southern United States is an important accomplishment since it may help to develop more specific biological control strategies aimed at protecting wild cactus from this mealybug. In classical biological control programs, the correct identification of the target species is a key issue for searching for natural enemies of the pest in its native area (Hoelmer & Kirk, 2005). Thus, untangling the evolutionary history of the H. pungens species complex did not only have taxonomic and systematic relevance, but from a practical perspective, it indicated that the design of biological control strategies (e.g., search for natural enemies) against the pest should focus on southeastern Brazilian cactus feeding mealybugs.
Our results showed that Amaranthaceae and/or Portulacaceae feeding mealybugs collected in Puerto Rico and continental United States were also derived from Amaranthaceae and/or Portulacaceae feedingHypogeococcus , though, in this case, from northeastern Brazil (Figures 2 and 3). These findings suggested two invasion events for mealybugs of the H. pungens species complex into Puerto Rico and the continental United States, one involving cactus feeders and the other mealybugs feeding on Amaranthaceae and/or Portulacaceae. Comparisons of the levels of genetic diversity in the native and invasive ranges of these mealybugs supported the idea of the occurrence of founder events during the colonization of Puerto Rico and southern United States. In both cases, introduced populations showed lower levels of genetic diversity in both mtDNA and nuDNA than in the respective native ranges, suggesting that a reduced number of individuals were involved in each colonization process (Table 1). Many invasive species have been capable of thriving in novel environments despite the reduction of genetic variation as a consequence of founder events that may negatively impact fitness, survival, and evolutionary potential of the invasive populations (Tsutsui, Suarez, Holway, & Case, 2000; Logan, Minnaar, Keegan, & Clusella‐Trullaset, 2020; Koch et al., 2020). In this vein, two putative species of the H. pungens complex have been successful invaders and continue to spread throughout the Caribbean and southern United States, threatening native species and cactus diversity despite the loss of genetic variation.
ACKNOWLEDGMENTS
We thank Andrés Fernando Sánchez Restrepo and Nadia Jiménez for technical assistance, and Fabian Font for identification of the host plants. We appreciate the revision of Mayra Vidal who gave us important suggestions on the manuscript. Partial funding was obtained from USDA-APHIS Farm Bill 17-8130-0757-IA and 19-8130-0852-IA, and USDA-APHIS Biological Control Program 18-8130-0757-IA. Permits for fieldwork in Brazil were provided by the SisGen (A9273F3) and the IBAMA (16BR022349/DF - 18BR027829/DF). Permits from Puerto Rico were provided by the U.S Fish & Wildlife Service (41522-16-003), and Department of Natural and Environmental Resources (OV-1617-15). D.P.M. is recipient of a PhD scholarship and M.B.A. of a postdoctoral fellowship both awarded by CONICET. E.H. is a member of CONICET Carrera del Investigador Científico.