Spatial and temporal patterns of parthenogenesis and parasitism in the freshwater snail Melanoides tuberculata

The Red Queen hypothesis predicts that sex should be more common in populations heavily infested with parasites, than in those without. This hypothesis was investigated in the aquatic snail Melanoides tuberculata, in which both sexual and parthenogenetic individuals exist in natural populations, and some populations are heavily infested by trematodes. The presence of fertile males and the higher genetic diversity of bisexual populations are indicative of sexual reproduction. We compared sites in 1990, 1999, and 2001, and we looked for a positive correlation between male and parasite frequencies. Male frequency was not correlated with the frequency of individuals infected by trematodes. This lack of correlation was reconfirmed in a retrospective power analysis. In a period of 9 years, male frequencies decreased but infection levels increased. These results do not support the Red Queen hypothesis. In samples with high male frequency the number of embryos was low, perhaps indicating that males may have a negative effect on embryo numbers. This effect of males on fitness could perhaps suggest that the cost of sex is fewer embryos. The reduction in embryo numbers may also represent a trade-off between mating and egg production costs.     

Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance

Many invasive taxa are hybrids, but how hybridization boosts the invasive process remains poorly known. We address this question in the clonal freshwater snail Melanoides tuberculata from Martinique, using three parental and two hybrid lines. We combine an extensive field survey (1990-2003) and a quantitative genetic experiment to show that hybrid lines have outcompeted their parents in natural habitats, and that this increased invasiveness co-occurred with pronounced shifts in life-history traits, such as growth, fecundity and juvenile size. Given the little time between hybrid creation and sampling, and the moderate standing genetic variance for life-history traits in hybrids, we show that some of the observed trait changes between parents and hybrids were unlikely to arise only by continuous selection. We therefore suggest that a large part of hybrid advantage stems from immediate heterosis upon hybridization.     

Genetic similarity and diversity of parthenogenetic and bisexual populations of the freshwater snail Melanoides tuberculata (Gastropoda: Prosobranchia)

Genetic variability and similarity were analysed in four parthenogenetic and five bisexual populations of the snail Melanoides tuberculata found in Israel. Electrophoretic studies of six enzymatic systems revealed 28 zones of activity. The average genetic identity between populations was low—0.725. A particularly low similarity (0.628) was obtained between parthenogenetic populations, compared to the average of 0.822 observed among the bisexual ones. The percentage of fixed electrophoretic bands in parthenogens was 53.9% compared to 12.5% observed in bisexual populations. The diversity of parthenogenetic populations was found to be lower than those of bisexual. The amount of electrophoretic diversity between populations of the parthenogenetic group was found to be 80%, whereas within the bisexual group the diversity between populations was only 42%.     

Reproduction in the freshwater gastropod,Helisoma: involvement of prostaglandin in egg production

Summary

The introduction of nanogram quantities of prostaglandin E₂ (PGE₂) into the female genital opening of mated animals was found to increase both the number of egg masses produced and the number of eggs per mass. The intrahaemocoelic administration of a thousand-fold higher concentration of PGE₂ was without effect, suggesting an indirect role of prostaglandin(s) in the regulation of egg production.

Prostaglandin (PG) synthetase activity in both the bursa copulatrix and ovotestis varied with the reproductive status. High PG synthetase activity was present in virgin animals, and lower activity was found in mated animals.

Prostaglandins produced by the bursa copulatrix are proposed here to be involved in the production of a matedness factor, which acts upon the brain to initiate or modulate egg production. PG produced by the ovotestis may be involved in ovulation. A model is proposed for the involvement of PG in the regulation of reproduction in Helisoma.     

Microsatellite and morphological analysis of population structure in the parthenogenetic freshwater snail Melanoides tuberculata: insights into the creation of clonal variability

The distribution of variability was studied at various geographical scales in the tropical freshwater snail Melanoides tuberculata, in order to analyse the role of factors shaping this distribution, including the mating system and population dynamics. This parthenogenetic polyploid species reproduces mainly asexually, with males occurring at low frequency. About 800 individuals (38 sites) were sampled from Africa and the Middle East, where the species originated, and from recently colonized habitats in South and Central America, and especially the island of Martinique. We first described variation of general aspects and ornamentation of the shells. This analysis confirms the existence of discrete morphs. Second, individuals were studied at three microsatellite loci, showing that each morph is a genetic clone with some minor variation compatible with models of microsatellite evolution. The genetic analysis also showed much more variation within than between clones. However, two populations from Africa exhibited a large amount of variability, and a mixture of sexual and asexual reproduction might explain these genetic patterns. The worldwide distribution of variability is, therefore, compatible with the African origin of the species, and the introduction of a few clones in other parts of the world. These results also suggest that the distribution of variability in Martinique is influenced by flooding events, and that two morphs from Martinique can be interpreted as hybrids between two pre-existing morphs, based on morphological, genetic and geographical arguments.     

The influence of chemical cues and conspecific density on the temperature selection of a freshwater snail (Melanoides tuberculata)

1. The effects of predation risk (via chemical cues) and conspecific density on temperature selection of the freshwater snail Melanoides tuberculata were assessed within a circular thermal gradient.2. Chemical cues from crushed conspecifics elicited the strongest avoidance response of snails in isothermal conditions.3. Following the addition of chemical cues to the thermal gradient, snails became more active and did not exhibit significant preference for any area within the gradient. Thus, average selected temperatures were higher when exposed to chemical cues.4. Although average selected temperatures increased with density of snails within the gradient, differences among densities were non-significant.5. This species seems to modify its thermoregulatory behavior when exposed to chemical cues (i.e. predation risk) suggesting that snails favor predator avoidance over thermal selection when presented with both demands.     

Density and variability of dinucleotide microsatellites in the parthenogenetic polyploid snail Melanoides tuberculata

Characterization of microsatellites in the parthenogenetic polyploid snail Melanoides tuberculata revealed an unusual high density of dinucleotide repeats. Multiple banding patterns were obtained at these loci, and interpreted as a consequence of polyploidy. Microsatellite variability was low within, but high between, shell morphotypes. Genotypes were wholly transmitted from mothers to offspring. These results suggest that reproduction is strictly apomictic, and that shell morphotypes are genetic clones.     

Statistical discrimination of sex in Melanoides tuberculata (Gastropoda: Thiaridae)

Systematists may rely on morphometric differences among samples of specimens for the recognition of living and fossil species, even though morphometric differentiation may be caused by non-genetic factors, such as ecophenotypy, differential growth rates and taphonomic mixing. When genetic differences between sexes or among closely related species are expressed as differences in the morphology of the individual or population, potentially valuable information becomes available to the systematist for a variety of genetic and ecological investigations. We have studied the morphology of the freshwater snail Melanoides tuberculata (Muller, 1774) in Israel, where males occur in what would otherwise be normally parthenogenetic (all female) populations. In modern M. tuberculata, sex may be determined by observation of gonadal tissue; in fossil specimens, any classification according to sex must be accomplished using only preservable features of the mineralized shell. Previous research confirmed that in large samples, mean shell shape of male and female snails differed significantly, but the degree of difference was too small to identify the sex of any individual specimen. We apply a three stage process that results with a high degree of accuracy in the discrimination of individual M. tuberculata specimens by sex on the basis of continuous morphological characters: (1) measurement of many aspects of shell morphology of individuals of known sex, and stepwise discrimination to discover which of the variables, if any, contribute to the morphometric differentiation of males from females (one time only, for the species); (2) use of these selected variables in a clustering procedure to make a preliminary assignment of each specimen to sex; (3) use of cluster assignments in a discrimination procedure to optimally predict sex. For species that exhibit morphometric differences between two groups, and for which continuous morphometric variation precludes the a priori recognition of discrete clusters, this sequential procedure may be of broad applicability. These objective methods may be applied to the discrimination within any set of specimens for which the hypothesis of two, and only two, constituent groups may be entertained.     

Biosorption of Cadmium from Aqueous Solution by Shell Dust of the Fresh Water Snail Melanoides tuberculata

ABSTRACT The metal bioadsorption potential of shell dust of the freshwater snail Melanoides tuberculata (MTSD) was evaluated under laboratory conditions using cadmium as a model metal. As bioadsorbent, MTSD exhibited a biosorption capacity of 27.03 mg g^?1 at pH 6, indicating potential to remove cadmium from aqueous solution. The adsorption data fit more to the Langmuir (R² = 0.998) equation than the Freundlich (R² = 0.761) equation at equilibrium condition. The kinetics of biosorption followed the pseudo-second-order model (R² = 0.999) better than the Lagergren model (R² = 0.676), as was evident from the regression analysis. The presence of calcium ions appears to have facilitated ion exchange with cadmium along with the binding of different functional groups, as revealed through Fourier transform infrared (FT-IR) analysis. It is apparent from these observations that MTSD can act as low-cost and efficient bioadsorbent for cadmium bioremediation from aquatic habitats. Use of the shells of M. tuberculata for metal biosorption will promote the utility of a waste material of biological origin for bioremediation of heavy metals such as cadmium.     

Apparent competition through facilitation between Melanoides tuberculata and Biomphalaria glabrata and the control of schistosomiasis

Interactions between two species that result in reduced growth rates for both and extinction of one of the species are generally considered cases of asymmetric interspecific competition. Exploitative or interference competition is the usual mechanism invoked. Here we describe another mechanism producing the same result, named apparent competition through facilitation (ACF), observed between Melanoides tuberculata and Biomphalaria glabrata populations. The superior competitor actually gives some benefit to the other species, whose population becomes unstable with progressively increasing oscillations, leading to extinction. A model of ACF using difference equations suggests initial dynamics distinct from traditional interspecific competition. The dynamics of two freshwater snails in the field and in laboratory experiments suggest ACF, and these relations should be considered in studies of schistosomiasis control. ACF could occur in natural populations, but might have gone undetected because the final result is similar to traditional interspecific competition.     

Ovoviviparity and the structure of the brood pouch in Melanoides tuberculata (Gastropoda: Prosobranchia: Thiaridae)

The freshwater gastropod Melanoides tuberculata broods its young in a pouch located in the anterodorsal region of the head-foot. The wall of the brood pouch is composed of smooth muscle surrounded by connective tissue. The lumen of the brood pouch is incompletely partitioned by trabeculae, formed by extensions or folds in the chamber wall that are composed of smooth muscle, connective tissue, nonciliated squamous epithelial cells, and some storage cells containing lipid and glycogen. The lumen of the chamber also contains a few cells with storage products. The general absence of secretory cells suggests that embryos derive little nutrition from the mother, and therefore embryonic development is probably ovoviviparous. Embryos in various stages of development were found within brood pouches, with later stage embryos varying in size. There was a negative relationship between embryo size and number of embryos in the brood pouch.     

Euspermatozoa and paraspermatozoa of the relict cerithiacean gastropod,Campanile symbolicum (prosobranchia,mesogastropoda)

Euspermatozoa and paraspermatozoa ofCampanile symbolicum Iredale, 1917 — a large, relict cerithiacean from Western Australia — have been examined using transmission electron microscopy and phase-contrast light microscopy. The euspermatozoa resemble those of many other mesogastropods with the important exception that the midpiece region exhibits unusual and possibly unique features. These include possession of seven or eight straight, periaxonemal elements (each containing scattered cristae) and a closely associated sheath composed of electrondense segments which are semicylindrical in shape and longitudinally aligned. This sheath — here termed the accessory midpiece sheath-surrounds only one half of the periaxonemal midpiece elements and lies outside the mitochondrial membrane (but nevertheless within the plasma membrane). Two types of paraspermatozoa occur inCampanile: (1) those with a nuclear core within the mosaic sheath of the head (nucleate paraspermatozoa) and (2) those lacking a nuclear core (dense blocks of mosaic sheath surrounding one to three axonemes — anucleate paraspermatozoa). An acrosome-like structure forms the apex of the head in both types of paraspermatozoa, while beyond the head region, electron-dense glycogen deposits are associated with each of the multiple tails. While the form ofCampanile paraspermatozoa suggests links with families such as the Cerithiidae, Potamididae and Turritellidae, the highly unusual morphology of the euspermatozoan midpiece indicates that the Campanilidae should occupy an isolated position within the superfamily Cerithiacea.     

Reproductive condition in two Malayan freshwater viviparid gastropods

Siamopaludina martensi and Filopaludina sumatrensis have typical viviparid reproductive systems with dimorphic spermatozoa and copulatory right tentacle in the male, and a large pallial brood-pouch in the female. Females outnumber males as in several other viviparids. Brood-pouches contained overall monthly averages of 0–14 developing young in S. martensi , 9–23 in F. sumatrensis , more than half of which were well-developed, later juveniles. Brood-pouch counts and ovary condition of both species varied in broad accordance with monthly rainfall, giving an irregularly seasonal pattern of annual change resembling those of several terrestrial Malayan snails. Juveniles emerge from the brood-pouch mostly at night. Alteration of aquarium conditions leads to temporarily accelerated release of young but does not permanently raise brood-pouch counts or rates of release.     

Focal Philophthalmus gralli infection possibly persists in Melanoides tuberculata over two years following the definitive hosts' removal

Philophthalmosis is a zoonotic disease associated largely with the spread of the invasive freshwater snail Melanoides tuberculata, serving as an intermediate host. Here we examined Philophthalmus gralli focal fenced infection site reported recently as being associated with Tinamus major and M. tuberculata in Alajuela, Costa Rica. Removal of the definitive hosts allowed us to address also the long-term survival strategy of the parasite. Initially, the snail intermediate hosts displayed high prevalence of P. gralli infection across all its age cohorts. Two years following the removal of definitive hosts, the infection rate decreased by one order of magnitude, while the snails aging less than one year displayed zero infection prevalence. Additionally, phylogenetic analysis of mitochondrial (ND1) and nuclear (ITS1, ITS2) DNA loci revealed negligible intrasite DNA variability of the specimens obtained at the study site in Costa Rica (but not of those obtained earlier in Peru or New Zealand), supporting strongly the hypothesis on focal origin of the infection. The observed dynamics of infection suggests the explanation for the high variability in P. gralli prevalence in intermediate hosts experienced worldwide. We noticed that the reports claiming > 20% prevalence of M. tuberculata infection by P. gralli originated exclusively from foci with known eye infection of the definitive hosts, while the P. gralli infection penetrance < 2% is typically associated with sites, where the infection of definitive hosts was not observed, suggesting that the infected definitive hosts were present onsite only in the past, or were present only at a site upstream or downstream of the respective sampling site. Thus, this is the first evidence on the possible persistence of eye-trematode infection site for over two years following the last confirmed outbreak in its adult hosts.     

In vitro effects of triclosan and methyl-triclosan on the marine gastropod Haliotis tuberculata

Triclosan (2,4,4'-trichloro-2'-hydroxy-diphenyl ether; TCS) is an antibacterial agent incorporated in a wide variety of household and personal care products. Because of its partial elimination in sewage treatment plants, TCS is commonly detected in natural waters and sediments. Moreover, due to its high hydrophobicity, TCS accumulates in fatty tissues in various aquatic organisms. TCS can be converted into methyl-triclosan (2,4,4'-trichloro-2'-methoxydiphenyl ether; MTCS) after biological methylation. In this study, the acute cytotoxicity of TCS and MTCS in short-term in vitro experiments was assessed on cell cultures from the European abalone Haliotis tuberculata. The results showed that morphology and density of hemocyte are affected from a concentration of 8 μM TCS. Using the XTT reduction assay, TCS has been demonstrated to decrease hemocyte metabolism activity in a dose- and time-dependent exposure. The IC(50) was evaluated at 6 μM for both hemocyte and gill cells after a 24 h-incubation with TCS. A significant cytotoxicity of MTCS was also observed from 4 μM in 24 h-old hemocyte culture. Our results reveal a toxic effect of TCS and MTCS on immune (hemocytes) and/or respiratory cells (gill cells) of the abalone, species living in coastal waters areas and exposed to anthropogenic pollution.     

Variation of shell shape in the clonal snail Melanoides tuberculata and its consequences for the interpretation of fossil series

Interpreting paleontological data is difficult because the genetic nature of observed morphological variation is generally unknown. Indeed, it is hardly possible to distinguish among several sources of morphological variation including phenotypic plasticity, sexual dimorphism, within-species genetic variation or differences among species. This can be addressed using fossil organisms with recent representatives. The freshwater snail Melanoides tuberculata ranks in this category. A fossil series of this and other species have been studied in the Turkana Basin (Kenya) and is presented as one of the best examples illustrating the punctuated pattern of evolution by the tenants of this theory. Melanoides tuberculata today occupies most of the tropics. We studied variation of shell shape in natural populations of this parthenogenetic snail using Raup's model of shell coiling. We considered different sources of variation on estimates of three relevant parameters of Raup's model: (1) variation in shell shape was detected among clones, and had both genetic and environmental bases; (2) sexual dimorphism, in those clones in which males occur, appeared as an additional source of shell variation; and (3) ecophenotypic variation was detected by comparing samples from different sites and years within two clones. We then tested the performance of discriminant function analyses, a classical tool in paleontological studies, using several datasets. Although the three sources of variation cited above contributed significantly to the observed morphological variance, they could not be detected without a priori knowledge of the biological entities studied. However, it was possible to distinguish between M. tuberculata and a related thiarid species using these analyses. Overall, this suggests that the tools classically used in paleontological studies are poorly efficient when distinguishing between important sources of within-species variation. Our study also gives some empirical bases to the doubts cast on the interpretation of the molluscan series of the Turkana Basin.     

Cleavage pattern in embryos of Haliotis tuberculata (Archaeogastropoda) and gastropod phylogeny

The early cleavage pattern in embryos of the archaeogastropod Haliotis tuberculata strongly resembles the cleavage pattern of the archaeogastropods Trochus and Patella. It typically deviates from the cleavage patterns found in embryos of more advanced Archaeogastropoda, Caenogastropoda (the majority of the meso- and neogastropods), and Euthyneura (opisthobranch and pulmonate gastropods). It is assumed that the cleavage pattern found in Haliotis, Trochus, and Patella represents the ancestral pattern. A regular pattern of heterochronic changes in the succession of the formation of the larval trochoblasts and the stem cell of the adult mesoderm can be observed from the more primitive Archaeogastropoda to the more advanced Euthyneura. This observation strengthens the idea that the early cleavage pattern contains significant phyletic information. © 1993 Wiley-Liss, Inc.     

Melanoides tuberculata (Mollusca: Thiaridae) harboring renicolid cercariae (Trematoda: Renicolidae) in Brazil

Melanoides tuberculata , naturally infected by gymnocephalous cercariae, were found in aquatic collections from Belo Horizonte, Minas Gerais, Brazil. After morphological characterization, larvae were used for experimental infection of Poecilia reticulata. Metacercariae were obtained from the liver of these fish, which were also found to be naturally infected in the same locality. The morphology and biology of the developmental stages of trematodes we obtained were characteristic of Renicola sp. This is the first record of renicolid cercariae and metacercariae in Brazil.