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.