Hybridization of Two Major Termite Invaders as a Consequence of Human Activity

March Hybridization of Two Major Termite Invaders as a Consequence of Human Activity Thomas Chouvenc 0 1 Ericka E. Helmick 0 1 Nan-Yao Su 0 1 0 1 Department of Entomology and Nematology, Fort Lauderdale Research and Education Center, University of Florida, Institute of Food and Agricultural Sciences, Fort Lauderdale, Florida, United States of America, 2 Department of Plant Pathology, Fort Lauderdale Research and Education Center, University of Florida, Institute of Food and Agricultural Sciences , Fort Lauderdale, Florida , United States of America 1 Academic Editor: Alex Cordoba-Aguilar, Universidad Nacional Autonoma de Mexico , MEXICO While hybridization of an invasive species with a native species is a common occurrence, hybridization between two invasive species is rare. Formosan subterranean termites (Coptotermes formosanus) and Asian subterranean termites (C. gestroi) are both ecologically successful and are the two most economically important termite pests in the world. Both species have spread throughout many areas of the world due to human activity; however, their distributions overlap in only three narrow areas because of distinct ecological requirements. In south Florida, where C. formosanus and C. gestroi are both invasive, the dispersal flight seasons of both species overlapped for the first time on record in 2013 and 2014. Pairings of heterospecific individuals were readily observed in the field and C. gestroi males preferentially engaged in mating behavior with C. formosanus females rather than females from their own species. In the laboratory, heterospecific and conspecific pairings had an equal colony establishment rate, but heterospecific incipient colonies had twice the growth rate of conspecific incipient colonies, suggesting a potential case of hybrid vigor. As all prezygotic barriers were lifted between the two species in the field, the apparent absence of post-zygotic barriers in the laboratory raises the possibility for introgressive hybridization in south Florida. While laboratory observations remain to be confirmed in the field, and the alate hybrid fertility is currently unknown, our results raise a tangible concern about the hybridization of two major destructive pest species. Such hybridization would likely be associated with a new economic impact. - Competing Interests: The authors have declared that no competing interests exist. Habitat alteration and human transportation have favored the spread of species with invasive capabilities as they may easily adapt to modified niches [13]. The establishment of invasive organisms in non-native areas can result in heterospecific interactions between invasive and native species, with potential for hybridization [4]. Introgression resulting from such hybridization can have important ecological and evolutionary consequences on native populations [58], and often are facilitated by human activity [4,9]. There is also mounting evidence that warming environments resulting from climate change can be an important factor contributing to such hybridization, either by altering the species distribution, or temporally shifting the mating season of species [10]. While the hybridization of non-native species with native species has been documented in a wide range of organisms [11,12], including plants [13], amphibians [14], fishes [15], mammals [16] and insects [17], few cases of hybridization involving two invasive species in non-native areas have been described. One such case is the hybridization of two invasive fire ant species (Solenopsis invicta S. richteri) where a hybrid zone is now fully established in the Southern United States [18,19]. To a lesser extent, gene introgression from the Africanized honey bee to European honey bee populations (Apis mellifera subspecies) has become a problem for human activity in North and South America [20]. Hybrid introgressions among non-native organisms have only been described in a couple of social insects with socioeconomic impacts. Here, we describe a potentially new case of hybridization between two invaders in another social insect group with major economic importance. Many subterranean termite (Isoptera: Rhinotermitidae) species are considered urban pests due to their tendency to attack man-made structures [21], and some are now invasive throughout the world, increasingly causing structural damage [22]. The Formosan subterranean termite (Coptotermes formosanus) and the Asian subterranean termite (C. gestroi) are the two most destructive structural pests in the world and are responsible for most of the $40 billion annual economic impact from termite damage [21]. As social insects, mature Coptotermes colonies can reach more than a million individuals [23] with caste polymorphism and polyethism [24], and have underground foraging galleries reaching up to 100 m, making detection and control difficult [25,26]. Coptotermes formosanus is endemic to China and Taiwan and has spread to many temperate and subtropical regions of the world [22]. It is now found throughout the southeastern United States and is responsible for more than $1 billion of structural damage each year in the United States alone [27]. Coptotermes gestroi is native to southeast Asia and has spread in many tropical regions, being potentially the most ubiquitous and destructive subterranean termite pest in the world [22]. Both species have distinct ecological requirements [28], but there are now established populations in many non-native areas due to human activity [29]. This observation reflects the current global biotic homogenization of some ecosystems, i.e. the replacement of native biotas by a small group of expanding non-native species in many parts of the world [30,31]. Their distributions now overlap in three narrow locations of the world [32,33]: the south part of the island of Taiwan, the island of Oahu in Hawaii, and southeast Florida (Fig. 1). However, studies concerning the interaction between C. formosanus and C. gestroi are restricted to competition between workers and soldiers from mature colonies, where individuals displayed interspecies agonism and competed for the access to resources [28,34]. The interspecies interactions of individuals from the reproductive caste (alates) have not yet been investigated. Swarming events (dispersal flights) in Coptotermes consist of mature colonies seasonally emitting thousands of alates at dusk [35]. Individuals drop their wings after the dispersal flight, find a mate, and engage in tandem behavior. The tandem behavior is initiated by the male as he maintains contact with the tip of the females abdomen [36]. The female then leads the way in search of a favorable nesting site, in which both individuals seclude themselves and establish the incipient colony [37]. It takes up to 8 yrs for these colonies to mature and initiate dispersal flights [38]. In south Florida, it was documented that the two species have distinct dispersal flight seasons [35]; h (...truncated)