Introgressive hybridization between two non‐native apple snails in China: widespread hybridization and homogenization in egg morphology

Abstract

BACKGROUND: Apple snails from the genus Pomacea have spread widely in paddy fields and other wetlands of southern China since their introduction in the 1980s. Pomacea spp. are commonly identified using mitochondrial COI sequences. However, sequencing the nuclear elongation factor 1-alpha (EF1⊍) gene revealed genetic introgression between field populations of P. canaliculata and P. maculata, which produce surviving hybrids in laboratory crossbreeding experiments. RESULTS: In this study, we sequenced 1054 EF1⊍ clones to design specific primers and established a fast and accurate multiplex polymerase chain reaction (PCR) method for genotyping EF1⊍. Combined with genotyping P. canaliculata and P. maculata based on mitochondrial COI and nuclear EF1⊍, we revealed the genetic introgression patterns of 30 apple snail populations in China. Purebred and hybrid individuals of P. canaliculata were widely distributed, while pure maculata-EF1⊍ type was detected only in a few individuals identified as P. canaliculata based on COI sequences. Each egg clutch had one to three genetic patterns, indicating multiple paternity or segregation in the progeny of hybrids. The higher percentages of hybrids in both wild populations and progeny than the homozygotes indicated a potential heterosis in the apple snail populations. Additionally, egg size and clutch size of the apple snails became homogeneous among the non-native populations exhibiting introgression hybridization. CONCLUSION: Our findings emphasize the value of apple snails as a model to study the mechanisms and impacts of introgressive hybridization on fitness traits.

Molecular analyses revealed three morphologically similar species of non‐native apple snails and their patterns of distribution in freshwater wetlands of Hong Kong

“…Individuals with inconsistent identification based on the two genes were hybrids. We genotyped the nuclear EF1α gene for each snail collected from Hong Kong and diagnosed as P. canaliculata or P. maculata using the primer‐specific‐multiplex PCR described by Yang et al (2020). Although a previous study based on the EF1α gene indicated incomplete lineage sorting between P. occulta and P. canaliculata and P. maculata (Yang et al, 2019), we also genotyped the EF1α gene of the snails with a COI type of P. occulta to check the hybridization patterns among these species.…”

“…Although a previous study based on the EF1α gene indicated incomplete lineage sorting between P. occulta and P. canaliculata and P. maculata (Yang et al, 2019), we also genotyped the EF1α gene of the snails with a COI type of P. occulta to check the hybridization patterns among these species. The multiplex PCR assay included two pairs of specific primers (Appendix : Table S1), including EF3Fc/EF3Rc targeting on a 125 bp of canaliculata‐EF1α, and EF1Fm/EF3Rm targeting on a 151 bp of maculata‐EF1α (Yang et al, 2020). We performed PCR in 25 μl solution containing 12.5 μl Premix Taq ™ (Takara), 1 μl each primer (10 mM), 1 μl template DNA, and 7.5 μl ddH 2 O.…”

“…We included sequences of apple snails from Malaysia because it provides the only country with recent COI gene data on apple snails (Kannan et al, 2020; Rama Rao et al, 2018). Moreover, because introgressive hybridization between Pomacea species has been detected in both Asia and their native ranges (Glasheen et al, 2020; Matsukura et al, 2013; Yang et al, 2020; Yoshida et al, 2014), we also analysed the hybridization patterns of apple snails collected from Hong Kong through genotyping the nuclear elongation factor 1‐alpha (EF1α) gene.…”

Genetic diversity analysis of the invasive gall pest Leptocybe invasa (Hymenoptera: Apodemidae) from China

“…Hybridization is considered to be an important driving force for the adaptive evolution of species [ 22 , 23 ]. Introgression caused by hybridization has been reported in many animals, such as insects [ 24 ], mollusks [ 25 ], mammals [ 26 ], reptiles [ 27 ], amphibians [ 28 ], and fish [ 29 ]. In recent decades, with the frequent occurrence of invasive species introduction events, hybridization opportunities between invasive species and their relatives have increased, and introgressive hybridization progeny may be more invasive, leading to the extinction of local parent groups [ 30 , 31 ].…”

Niche conservatism and invasion potential of Pomacea canaliculata and Pomacea maculata in two invaded regions

“…In east and south-east Asia, the apple snails have invaded a wide range from tropical to temperate regions after several introductions(Hayes et al 2008), northern expansion of this species were determined by low temperature during winter(Ito 2002;Syobu et al 2001). Compared with P. canaliculata, P. maculata has poorer tolerance of both cold and desiccation(Yang et al 2020), which was re ected in its distribution in southern, western coastal regions and Florida in US. These ndings on difference in ecophysiological tolerances of the two Pomacea snails, has implications for understanding differential spread potentials in the invasive range.…”