The apple snails Pomacea canaliculata, Pomacea diffusa and Pomacea maculate (Gastropoda: Caenogastropoda: Ampullariidae) are invasive pests causing massive economic losses and ecological damage. We sequenced and characterized the complete mitochondrial genomes of these snails to conduct phylogenetic analyses based on comparisons with the mitochondrial protein coding sequences of 47 Caenogastropoda species. The gene arrangements, distribution and content were canonically identical and consistent with typical Mollusca except for the tRNA-Gln absent in P. diffusa. An identifiable control region (d-loop) was absent. Bayesian phylogenetic analysis indicated that all the Ampullariidae species clustered on the same branch. The genus Pomacea clustered together and then with the genus Marisa. The orders Architaenioglossa and Sorbeoconcha clustered together and then with the order Hypsogastropoda. Furthermore, the intergenic and interspecific taxonomic positions were defined. Unexpectedly, Ceraesignum maximum, Dendropoma gregarium, Eualetes tulipa and Thylacodes squamigerus, traditionally classified in order Hypsogastropoda, were isolated from the order Hypsogastropoda in the most external branch of the Bayesian inference tree. The divergence times of the Caenogastropoda indicated that their evolutionary process covered four geological epochs that included the Quaternary, Neogene, Paleogene and Cretaceous periods. This study will facilitate further investigation of species identification to aid in the implementation of effective management and control strategies of these invasive species.

The successful establishment of invasive populations is closely linked to environmental factors. It is unclear whether coexisting species in the native area follow the same genetic pattern in the invaded continents under the local climate factors. Two coexisting morphologically similar snails (Pomacea canaliculata and P. maculata), native to tropical and sub-tropical South America, have become invasive species for agriculture production and wetland conservation across five continents over 40 years. We analyzed the correlation between the genetic diversity of the two snails and the climate factors or habitat changes. Based on the 962 sequences from the invaded continents and South America, the nucleotide diversity in the agricultural habitat was low for P. canaliculata, whereas it was high for P. maculata, compared with that in the non-agricultural habitat. The two snails showed a divided population structure among the five continents. The P. canaliculata population in the invaded continents has remained stable, whereas the P. maculata population expanded suddenly. Seven main haplotype networks and two ancestral haplotypes (Pc3, Pm1) were found in the P. canaliculata and P. maculata populations. The haplotypes of the two snails were related to local climate factors. The overall fixation index of P. canaliculata and P. maculata was 0.2657 and 0.3097 between the invaded continents and South America. The population expansion of the two snails fitted the isolation-by-distance model. We discovered nine new sequences from the sampling locations. Overall, the genetic diversity and genetic differentiation of the two invasive snails were closely related to geographic separation, agricultural habitat, and climate factors.