Ongoing human-mediated spread and hybridization of two major invasive termite species

Abstract

Human-mediated biological invasions can lead to introgressive hybridization events between lineages that have evolved independently, with potential for evolutionary, ecological, economic and social impacts. This study provides evidence for the ongoing spread and hybridization between two major invasive and destructive termite pest species, Coptotermes gestroi and C. formosanus in Florida. Heterospecific courtship behaviour between alates (winged reproductive caste) of the two species has led to the establishment of F1 hybrid colonies in the field, which have matured and produced F1 hybrid alates. Laboratory backcross attempts confirmed the possibility for F1 hybrid female alates to establish viable F2 colonies with males of either parental species. With the recent documentation of introgressive hybridization between the two species in Taiwan, the current study confirms its independent occurrence in Florida, demonstrating that both Coptotermes species can hybridize in areas where their distributions overlap. In Florida, the proximity of field-established hybrid colonies to the large leisure boat industry implies that Florida populations of C. gestroi, C. formosanus and their hybrids will continue to serve as a bridgehead source of propagules for further dispersal beyond their current distribution, with a potential for F1 hybrids to spread outside of Florida.

Keywords: anthropomorphic dispersal; biological invasion; hybridization; termite.

Figure 1.

Estimated distribution of Coptotermes spp. in areas with documented distribution overlap of C. gestroi and C. formosanus, as of July 2024. Modified from [45,48,49] and according to updated records from the University of Florida Termite Collection. Scale indicates latitude.

Figure 2.

Coptotermes alate morphology, phenology and genotype. (A) Focus on the antennal spot morphology (arrows point to respective inset images at scale 2×). The C. formosanus spot is poorly defined. There is a defined crescent antennal spot for C. gestroi, and there is an enlarged antennal spot for atypical alates. (B) Intermediate colour hue in the atypical alate dorsal abdomen (live individuals) compared with parental species, here all females. (C) Dispersal flight phenology (daily average number of collected alates, on a log+1 scale, over the 2022−2024 seasons) of the three alate morphotypes. (D) Results from a STRUCTURE analysis of microsatellites (169 individuals collected in 2021−2023, k = 2, loci = 3), and their maternal lineage (CoII gene), confirming that atypical alates were produced by field-established Hybrid F and Hybrid G colonies in Florida since at least 2021. The proportional assignment of ancestry from the admixture model is bound to approximately 92.7% certainty for parental species owing to the use of only three loci in the analysis, although sufficient to confirm hybridization. CG = C. gestroi, CF = C. formosanus, HyG = F1 Hybrid G, HyF = F1 Hybrid F.

Figure 3.

F2 hybrid colonies characteristics. (A) Colony survival and growth 1 year after establishment in laboratory conditions (ANOVA, F = 28.81, d.f. = 4, p < 0.001, different letters indicate significant difference in colony growth with a Tukey’s HSD test, n/a = not applicable). (B) Colony survival and growth 2 years after establishment in laboratory conditions (ANOVA, F = 8.07, d.f. = 3, p < 0.001, Tukey’s HSD test). (C) Results from a STRUCTURE analysis of microsatellites for 190 workers collected from 23 laboratory colonies ( k = 2, loci = 3), and their maternal lineage (CoII gene), confirming that F1 hybrid female alates can produce viable offspring when backcrossed with either parental species. For F2 workers, individuals from a given colony are ranked in order of ancestry assignment towards the species the hybrid female backcrossed with, to visually determine each colony of origin (4 ‘F2 Hybrid HG’ colonies and 7 ‘F2 Hybrid HF’ colonies). CG = C. gestroi, CF = C. formosanus, HyG = ‘F1 Hybrid G’, HyF = ‘F1 Hybrid F’, ‘F2 Hyb HG’ = HY × CG and ‘F2 Hyb HF’ = HY × CF. (D) Ventral morphology of F2 soldier head capsule displaying faint striations (st) beside the postmental sulcus. (E) Lateral morphology of F2 soldier head capsule displaying a prominent dorsal bulging vertex (bv) and two pairs of setae beside the fontanelle (se). (f) Frontal morphology of six different F2 soldier head capsules displaying highly variable fontanelle shapes (fo) that overlap with soldier morphology from both parental species and F1 hybrids.

Figure 4.

Confirmation of a Coptotermes hybrid colony established in the field, in Ft Lauderdale, Florida city. Soldiers collected from two trees located 22 m apart were confirmed to be F1 Hybrid G termites, putatively from the same colony. This park is located within a boat marina where private vessels with maritime capabilities are moored or docked throughout the year. This situation reflects the potential for vessels to be infested by either Coptotermes species or their hybrids over time as they come and go, making such a location a functional bridgehead for the further spread of Coptotermes in other parts of the world.