Hybrids of two destructive subterranean termites established in the field, revealing a potential for gene flow between species

Abstract

Hybridization between invasive pest species may lead to significant genetic and economic impacts that require close monitoring. The two most invasive and destructive termite species worldwide, Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann), have the potential for hybridization in the field. A three-year field survey conducted during the dispersal flight season of Coptotermes in Taiwan identified alates with atypical morphology, which were confirmed as hybrids of the two Coptotermes species using microsatellite and mitochondrial analyses. Out of 27,601 alates collected over three years, 4.4% were confirmed as hybrid alates, and some advanced hybrids (>F1 generations) were identified. The hybrid alates had a dispersal flight season that overlapped with the two parental species 13 out of 15 times. Most of the hybrid alates were females, implying that mating opportunities beyond F1 may primarily be possible through female hybrids. However, the incipient colony growth results from all potential mating combinations suggest that only backcross colonies with hybrid males could sometimes lead to brood development. The observed asymmetrical viability and fertility of hybrid alates may critically reduce the probability of advanced-hybrid colonies being established in the field.

Fig. 1. Distribution of the Coptotermes spp. in Taiwan according to NCHU Termite Collection between 2005 to 2020.

Locations where natural hybrids were found were denoted as a red triangle and a red cross. Both locations are located in Taichung city, the northern part of the sympatric area.

Fig. 2. Facial morphology of C. formosanus, C. gestroi and the putative hybrids.

A C. formosanus, head saddle brown, no antennal spots or only dim patches. B C. gestroi, head coconut brown (darker brown) with apparent antennal spots. C The putative hybrids, head saddle brown with apparent antennal spots. D Morphometric distribution of Taiwanese Coptotermes alates. The unit of both axes is the light intensity value measured under the 8-bit RGB color model. The brightness of head (x axes) was obtained by summing RGB values, and the contrast between head and antennal spots (y axes) was quantified through the Euclidean distance between the RGB value of head and spot.The same capital letter after the measurements are not significantly different at the α = 0.05 level for each character. E The antennal spot of C. formosanus, the border of the spot blurry, and if present, both the dorsal and the ventral borders convex. F The antennal spot of C. gestroi and the putative hybrids, with the dorsal border convex and the ventral border concave. G C. gestroi and the putative hybrids showed a distinct thickness of the antennal spots.

Fig. 3. Species clustering and detection of advanced hybrids.

A The result of STRUCTURE analysis for K = 2 (middle), side by side with individual morphological type (top) and their maternal lineage (below). The result referred to the two morphological types to the two species: the color gray represents the genetic composition from C. formosanus, and the color black represents the genetic composition from C. gestroi. The putative hybrids carried about half the proportion from each cluster, accompanied by mitochondria inherited from either species, which demonstrates they are the hybrids of the two parental species. The advanced hybrids were marked with number. B The alleles of three microsatellite markers of the four advanced hybrids were shown, and the species’ private alleles were marked with color. These individuals had alleles on one locus originating from the same species (same color).

Fig. 4. Time series of dispersal flight events by fitting occurrences to Gaussian functions.

Each curve, C. formosanus (yellow), C. gestroi (blue), and the hybrid (red), presented one single peak. Arrows point out the timing that the peak value occurred. Gaussian function summarized the curves with three parameters, including p, the peak value of the occurrence; T, the timing that the peak value occurred; and d, the deviation that controls the slope of the peak.

Fig. 5. Reproductive performance of the incipient colonies.

A The average number of matured ovariole before paring. B The average number of eggs after eight days of rearing. C The average number of matured ovariole after 54 days of rearing. D The average number of offspring after 54 days of rearing. Comparisons were done using the Kruskal–Wallis test followed by Mann–Whitney pairwise test by Bonferroni-corrected p values. When columns are marked as the same letter, the means are not significantly different at the alpha = 0.05. The paring combinations were abbreviated as female × male. CF C. formosanus, CG C. gestroi, HY hybrid.