Apple snails (Ampullariidae: Pomacea) native to the New World have become agricultural and environmental pests widely in southern and eastern Asia since their introduction in about 1980. Although their impacts have been extensively documented, considerable confusion persists regarding their identities and geographical origins. Efforts to resolve the confusion have suffered from inadequate taxonomic and geographical sampling from both native and introduced ranges. Using phylogenetic and genealogical methods, we analysed 610–655 bp of cytochrome c oxidase subunit I DNA sequences from 783 apple snails from 164 Asian locations and 57 native South American locations. In Asia, we found four species of Pomacea in two clades: (1) Pomacea canaliculata and P. insularum, and (2) P. scalaris and P. diffusa. Parsimony networks and mismatch distributions indicate that the non‐native ranges of the two most widespread species, P. canaliculata and P. insularum, probably result from multiple introductions. Molecular analyses are consistent with early accounts; non‐native P. canaliculata populations trace back to multiple locations in Argentina and have probably been introduced more than once. In contrast, P. insularum was probably introduced from Brazil and Argentina independently. Multiple introductions may, in part, explain the success and rapid spread of these two species. Unlike P. canaliculata and P. insularum, P. scalaris and P. diffusa were probably introduced through the aquarium trade, derived originally from Argentina and Brazil, respectively. Possible physiological, ecological, and native range differences among these four species highlight the importance of accurate identification in understanding invasion patterns and processes, which is vital in developing and implementing management strategies.

Abstract

Background

Since the mid 1990s populations of non-native apple snails (Ampullariidae) have been discovered with increasing frequency in the continental United States. Given the dramatic effects that introduced apple snails have had on both natural habitats and agricultural areas in Southeast Asia, their introduction to the mainland U.S. is cause for concern. We combine phylogenetic analyses of mtDNA sequences with examination of introduced populations and museum collections to clarify the identities, introduced distributions, geographical origins, and introduction histories of apple snails.

Results

Based on sampling to date, we conclude there are five species of non-native apple snails in the continental U.S. Most significantly, we recognize three species within what has been called the channeled apple snail: Pomacea canaliculata (California and Arizona), Pomacea insularum, (Florida, Texas, and Georgia) and Pomacea haustrum (Florida). The first established populations of P. haustrum were discovered in the late 1970s in Palm Beach County Florida, and have not spread appreciably in 30 years. In contrast, populations of P. insularum were established in Texas by 1989, in Florida by the mid to late 1990s, and in Georgia by 2005, and this species continues to spread rapidly. Most introduced P. insularum haplotypes are a close match to haplotypes from the Río Uruguay near Buenos Aires, indicating cold tolerance, with the potential to spread from Florida, Georgia, and Texas through Louisiana, Alabama, Mississippi, and South Carolina. Pomacea canaliculata populations were first discovered in California in 1997. Haplotypes of introduced P. canaliculata match native-range haplotypes from near Buenos Aires, Argentina, also indicating cold tolerance and the potential to establish farther north.

Conclusion

The term "channeled apple snail" is descriptive of a morphology found in many apple snail species. It does not identify a single species or a monophyletic group. Clarifying species identifications permits a more accurate assessment of introduction histories and distributions, and provides a very different picture of the tempo and pattern of invasions than was inferred when the three species with channeled sutures were considered one. Matching introduced and native-range haplotypes suggests the potential for range expansion, with implications for native aquatic ecosystems and species, agriculture, and human health.

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Ampullariidae comprises two lineages of freshwater gastropods: one Old World and one New World. Recent molecular work confirmed the monophyly of the family and began to clarify generic relationships, but current systematics remains unsatisfactory. With more than 300 available species group names for New World taxa alone, taxonomic confusion is rampant, as illustrated by two species that have been introduced widely and are difficult to differentiate conchologically, Pomacea maculata Perry, 1810 and Pomacea canaliculata (Lamarck, 1822). Misidentification hampers efforts to manage their spread and impacts as invasives, and prevents meaningful comparative analyses of their biology. Here we clarify the taxonomy, describe the morphological and genetic distinctiveness of the two species, and re-evaluate their biogeographic ranges. They differ most clearly genetically, with no shared haplotypes and a mean genetic distance of 0.135 at cytochrome c oxidase subunit I (COI). Differences in shell morphology are most obvious in recently hatched juveniles; the number of eggs per clutch is higher in P. maculata, and the individual eggs are smaller, so P. canaliculata hatchlings are nearly twice as large as those of P. maculata. Adult shells differ primarily in the angulation of the whorl shoulder and pigmentation of the inner pallial lip, with the latter a distinctive feature of P. maculata. They also differ in reproductive anatomy, most notably in P. canaliculata having two distinctive glandular tissues in the apical penial sheath gland, and P. maculata lacking a medial sheath gland but possessing a basal sheath gland. Pomacea canaliculata is restricted to a narrower southern range, whereas P. maculata ranges extensively throughout much of South America. Ampullaria gigas Spix, 1827 and Ampullaria insularum d'Orbigny, 1835 are herein synonymized with P. maculata. Neotypes are designated for P. maculata and A. gigas, and a lectotype is designated for A. insularum. A neotype is designated for P. canaliculata.

Eosinophilic meningitis caused by the parasitic nematode Angiostrongylus cantonensis is an emerging infectious disease with recent outbreaks primarily in tropical and subtropical locations around the world, including Hawaii. Humans contract the disease primarily through ingestion of infected gastropods, the intermediate hosts of Angiostrongylus cantonensis. Effective prevention of the disease and control of the spread of the parasite require a thorough understanding of the parasite's hosts, including their distributions, as well as the human and environmental factors that contribute to transmission. The aim of this study was to screen a large cross section of gastropod species throughout the main Hawaiian Islands to determine which act as hosts of Angiostrongylus cantonensis and to assess the parasite loads in these species. Molecular screening of 7 native and 30 non-native gastropod species revealed the presence of the parasite in 16 species (2 native, 14 non-native). Four of the species tested are newly recorded hosts, two species introduced to Hawaii (Oxychilus alliarius, Cyclotropis sp.) and two native species (Philonesia sp., Tornatellides sp.). Those species testing positive were from a wide diversity of heterobranch taxa as well as two distantly related caenogastropod taxa. Review of the global literature showed that many gastropod species from 34 additional families can also act as hosts. There was a wide range of parasite loads among and within species, with an estimated maximum of 2.8 million larvae in one individual of Laevicaulis alte. This knowledge of the intermediate host range of Angiostrongylus cantonensis and the range of parasite loads will permit more focused efforts to detect, monitor and control the most important hosts, thereby improving disease prevention in Hawaii as well as globally.

Apple snails (Ampullariidae) are a diverse family of pantropical freshwater snails and an important evolutionary link to the common ancestor of the largest group of living gastropods, the Caenogastropoda. A clear understanding of relationships within the Ampullariidae, and identification of their sister taxon, is therefore important for interpreting gastropod evolution in general. Unfortunately, the overall pattern has been clouded by confused systematics within the family and equivocal results regarding the family's sister group relationships. To clarify the relationships among ampullariid genera and to evaluate the influence of including or excluding possible sister taxa, we used data from five genes, three nuclear and two mitochondrial, from representatives of all nine extant ampullariid genera, and species of Viviparidae, Cyclophoridae, and Campanilidae, to reconstruct the phylogeny of apple snails, and determine their affinities to these possible sister groups. The results obtained indicate that the Old and New World ampullariids are reciprocally monophyletic with probable Gondwanan origins. All four Old World genera, Afropomus, Saulea, Pila, and Lanistes, were recovered as monophyletic, but only Asolene, Felipponea, and Pomella were monophyletic among the five New World genera, with Marisa paraphyletic and Pomacea polyphyletic. Estimates of divergence times among New World taxa suggest that diversification began shortly after the separation of Africa and South America and has probably been influenced by hydrogeological events over the last 90 Myr. The sister group of the Ampullariidae remains unresolved, but analyses omitting certain outgroup taxa suggest the need for dense taxonomic sampling to increase phylogenetic accuracy within the ingroup. The results obtained also indicate that defining the sister group of the Ampullariidae and clarifying relationships among basal caenogastropods will require increased taxon sampling within these four families, and synthesis of both morphological and molecular data.

The family Ampullariidae includes both aquatic and amphibious apple snails. They are an emerging model for evolutionary studies due to the high diversity, ancient history, and wide geographical distribution. Insight into drivers of ampullariid evolution is hampered, however, by the lack of genomic resources. Here, we report the genomes of four ampullariids spanning the Old World ( Lanistes nyassanus ) and New World ( Pomacea canaliculata , P. maculata , and Marisa cornuarietis ) clades. The ampullariid genomes have conserved ancient bilaterial karyotype features and a novel Hox gene cluster rearrangement, making them valuable in comparative genomic studies. They have expanded gene families related to environmental sensing and cellulose digestion, which may have facilitated some ampullarids to become notorious invasive pests. In the amphibious Pomacea , novel acquisition of an egg neurotoxin and a protein for making the calcareous eggshell may have been key adaptations enabling their transition from underwater to terrestrial egg deposition.

Molluscs constitute the second largest phylum in terms of the number of described species and possess a wide array of characteristics and adaptations for living in marine, terrestrial, and freshwater habitats. They are morphologically diverse and appear in the fossil record as far back as the early Cambrian (~560 mybp). Despite their high diversity and long evolutionary history, molluscs are often underused as models for the study of general aspects of evolutionary biology. Freshwater snails in the family Ampullariidae have a global tropical and subtropical distribution and high diversity with more than 150 species in nine currently recognized genera, making them an ideal group to address questions of historical biogeography and some of the underlying mechanisms of speciation. They exhibit a wide range of morphological, behavioral, and physiological adaptations that have probably played a role in the processes of diversifi cation. Here we review some of the salient aspects of ampullariid evolution and present some early results from ongoing research in order to illustrate the excellent opportunity that this group provides as a system for addressing numerous questions in evolutionary biology, particularly with regard to the generation of biodiversity and its distribution around the globe. Specifi cally, we suggest that ampullariids have great potential to inform (1) biogeography, both on a global scale and a smaller intra-continental scale, (2) speciation and the generation of biodiversity, through analysis of trophic relations and habitat partitioning, and addressing issues such as Rapoport's Rule and the latitudinal biodiversity gradient, and (3) the evolution of physiological and behavioral adaptations. Also, a number of species in the family have become highly successful invasives, providing unintentional experiments that may offer insights into rapid evolutionary changes that often accompany introductions, as well as illuminating invasion biology in general.