subtitle for learnabout section of A SNAIL'S ODYSSEY
  Reproduction & development
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  This section on reproduction & development is divided into topics of genetics, considered here, and MATE SELECTION & COPULATION, PATTERNS OF DEVELOPMENT, and DISPERSAL considered elsewhere.
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Research study 1

map with haplotype distributions for the direct-developing littorinid Littorina sitkanaWith their extensive north-south distributions and similar life styles, the several Littorina species on the west coast represent a nice model system to test the relationship between type of larval development and extent of genetic structure.  Molecular ecologists generally predict that marine invertebrates with planktonic larvae will have less genetic structure or diversity than ones with direct development.  Thus, because of greater genetic inter-mixing, the planktonic-developing Littorina scutulata and L. plena should show less genetic structure than the direct-developing L. sitkana and L. subrotundata.  However, results froom nucleotide1- sequencing analyses obtained from samples of the 4 species collected at different sites from Washington to the Aleutian Islands do not fully support the hypothesis, with L. sitkana being the main deviant (see map: only data for L. sitkana are shown). The authors provide the following details:

1) Littorina scutulata larvae are planktonic for 35-70d. As predicted, no significant population structure is revealed, presumably owing to the broad distribution of larvae and potentially high levels of gene flow among populations of this species.
2) Littorina plena larvae are also planktonic for 35-70d. Contrary to expectations, some weakly significant population structure is revealed.
3) Littorina subrotundata2 has direct development to crawl-away juveniles and, as predicted, shows more population genetic-structure than either of the planktonic-developing species.
4) Littorina sitkana has direct development to crawl-away juveniles and, surprisingly, shows essentially no population structure. It is represented by almost a single haplotype3 along the coast (see map).  This species represents a striking deviation from expectation and is explained by the authors as a possible result of rafting of eggs on storm-created bits of brown alga Fucus to which the eggs are often attached, leading to homogenisation of haplotype frequencies. Another possibility discussed by the authors is recent expansion of the species after the last glaciation from a single refugium4 (15-18,000yr BP).  Kyle & Boulding 2000 Mar Biol 137: 835.

NOTE1  using the mitochondrial cytochrome b gene

NOTE2  several new polymorphic microsatellite loci have been isolated for L. subrotundata, providing finer-scale resolution for metapopulation analyses.  Tie et al. 2000 Molec Ecol 9: 107.

NOTE3  a set of genes in each chromosome of the genome that tend to be transmitted as a unit to the next generation

NOTE4 at least one such refugium is thought to have existed through the last glaciation period on the east side of Graham Island in Haida Gwai, British Columbia.  Warner et al. 1982 Science 218: 675. The expansion of species from post-glaciation refugia is considered elsewhere in the ODYSSEY: LEARN ABOUT SEA CUCUMBERS: GENETIC DRIFT and LEARN ABOUT WHELKS: DISPERSAL, HETEROZYGOSITY, & GLACIAL REFUGIA

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Research study 2

photograph of Crepidula onyx courtesy Linda Schroeder and Pacific Northwest Shell Club, Seattle, WashingtonA study by researchers at the University of California, San Diego on the genetics of slipper limpets Crepidula onyx in Mission Bay, California reveals no significant spatial or temporal patterns.  The lack of population structure is thought by the authors to be  attributable to wholesale mixing of larvae in the Bay by tidal currents.  In this area, Crepidula larvae are free-living for about 3wk.  More interestingly, the authors find significant multilocus heterozygote deficiencies in all samples, including both sexes, and across all localities and seasons.  Selection against the heterozygotes appears to occur during the larval phase or perhaps during settlement and metamorphosis. Apparently, similar heterozygote deficiencies have been reported in other molluscs, such as oysters, scallops, mussels, clams, and various snails, but without satisfactory explanation.  As noted by the authors, these findings go against the notion of fitness traits being associated with heterozygosity.  The authors consider various  causes, including self-fertilisation, inbreeding, water chemisty, and other possibilities, but are unable to add anything new to explain this general molluscan conundrum.  Plutchak et al. 2006 J Moll Stud 72: 337. Photographs courtesy Linda Schroeder and Pacific Northwest Shell Club, Seattle, Washington PNWSC.

NOTE  the researchers describe spatial (6 sites) and temporal (3-4 seasons) differentiation at 16 polymorphic allozyme loci in adult snails

NOTE  this possibility is quickly dismissed by the authors, as C. onyx is a sequential hermaphrodite and is not sexually functional during the transitional phase between male and female.  In fact, the male part of the gonad basically “self-destructs” prior to the transformation

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Research study 3

map showing collecting sites for genetics study on littorinid snails Littorina keenaeA research project complementary to Research Study 1 above assesses genetic variability in the west-coast winkle Littorina keenae.  The authors sample snails from 13 sites from mid-Baja California to mid-Oregon and analyse for variations in mitochondrial ND6 and cytochrome b genes. Results show no significant spatial population differentiation anywhere along the west coast, not even at the recognised distributional boundary at Point Conception, California.  The researchers credit this single panmitic genetic structure to high gene flow resulting from a free-swimming larval stage.  Interestingly, one site at San Pedro, Baja California yields a significant population differentiation between the years 1996 and 2005, supporting an idea referred to as the “sweepstakes” hypothesis.  The temporal variation observed at this one site, in fact, is much greater than the entire spatial variation shown in the rest of the study. Lee & Boulding 2007 Mol Ecol 16: 3084.

NOTE  this biogeographic boundary exists because of sharp temperature gradients and offshore current deflection resulting from the predominant south-flowing California Current encountering a large cyclonic gyre called the Southern California Eddy.  The gyre retains water south of Point Conception and tends to inhibit northward larval transport

NOTE  to quote the authors: “when by chance nearly all of the progeny from an aggregation of highly fecund sisters that possess a rare haplotype successfully recruit to become the next generation, the rare haplotype can become temporarily common across the entire species’ range”

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Research study 4

histogram comparing genetic diversity in west-coast littorinid snails: 2 species Littorina scutulata and L. plena with planktotrophic larval development, and 2 species L. sitkana and L. subrotundata with direct development to crawl-away juvenilesResults of a follow-up study by the research group cited in Research Study 1 above confirm that the 2 west-coast littorinid species Littorina scutulata and L. plena with planktotrophic larval development have significantly greater genetic diversity than the 2 species Littorina sitkana and L. subrotundata with direct development in benthic egg masses that hatch to crawl-away juveniles (see histogram). This is contrary to the general belief by molecular ecologists that marine invertebrates with planktonic larvae will have less genetic diversity than ones with direct development, simply by the greater genetic mixing associated with planktonic dissemination.  Interestingly, and more in line with traditional thinking, the 2 poorly dispersing species L. sitkana and L. subrotundata exhibit significant spatial genetic structure over a certain small part of their distributional range (11-65km), not seen in the 2 planktotrophic species. However, when compared over a 10-yr period, the 2 planktotrophic species are found once again to exhibit greater temporal genetic structure than the 2 direct-developing species.  The unusual and seemingly contradictory nature of the results are explained by the authors in sweepstakes-theory terms related to high fecundity, broad larval dispersion during a 9-10wk planktonic life, but chancey survivorship after settlement in the planktotrophic-developing species.  In this idea, a few related females release their eggs at the same tim, and these and the resulting larvae are carried together in the same water currents to the same geographic locations, leading to population of several hundred km of coastline with genetically related individuals.  Thus, spatial genetic variance over 10s or even 100s of km would be relatively low, but temporal genetic variance could be relatively high.  It is a clever explanation for what otherwise seems a vexing conundrum.  Lee & Boulding 2009 Molec Ecol 18: 2165.

NOTE  the study is unique in that the authors compare genetic structure of closely related direct-developers and planktotrophic-developers over a 10-yr period using specimens collected from the same geographic sites

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Research study 5

diagram showing unique and shared haplotypes of winkles Littorina littorea among different locationsmap showing distributions of Littorina littorea in San Francisco BayA characteristic of recently introduced self-sustaining populations of non-native species is their generally low genetic diversity as compared with source populations.  Whether this is true for 3 populations of European winkles Littorina littorea in San Francisco and Anaheim Bays, California  is investigated by a research team from the Smithsonian Environmental Research Center, Maryland.  Results show the populations to contain only adult snails with high genetic diversity, rather than the usual bottleneck characteristics of recently introduced population (see map for distributions in San Francisco Bay).  The authors identify the California invasives as originating from the east coast of the U.S., probably in shipments of live seafood (see figure on Right for unique and shared haplotypes among regions).  The authors discuss possible reasons for lack of recruitment, focusing on higher than accustomed-to seawater temperatures as perhaps the most important.  The paper is interesting because it provides information on genetic characteristics of early-stage invasive populations that are not yet recruiting.  Chang et al. 2011 PLoS ONE 6 (1): e16035.

NOTE  sequencing of mitochondrial DNA in foot-muscle tissue

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