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Map of Mission Bay with locations of collection sites. Locality IB: Ingraham Bridge, NC: North Cove, SC: South Cove, VI: Vacation Isle, VB: Ventura Basin, PC: Perez Cove.
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Although the phenomenon of multilocus heterozygote deficiencies in numerous taxonomically diverse molluscs has been studied for over 30 years it has resisted general explanation. Here we describe a case in Crepidula onyx Sowerby, a common protandrous slipper limpet on the Pacific coast of southern California. Spatial and temporal differentiation at...
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... of C. onyx were collected from Mission Bay on the Pacific coast of southern California, approximately 22 km north of the U.S.-Mexico border (Fig. 1). Mission Bay is a man-made recreational area within the city of San Diego and lies on the former site of False Bay, a natural estuary at the mouth of the San Diego River. Covering over 1700 ha, the bay is now connected to the Pacific Ocean by a boat channel and the water (typically 3 m deep) is well mixed by tides and wind. Mean tidal ...
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... (neé McMeekin) collected C. onyx six localities ( Fig. 1) during three consecutive seasons: autumn 1984, winter 1985, spring 1985, hereafter referred to as the Autumn, Winter and Spring samples [season capitalized]. Ingraham Bridge is a rocky edge of a muddy channel located under the Ingraham street traffic-bridge on the north side of Vacation Isle. Snails were found on mussels on the bridge ...
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... by Woodruff et al. (1986), very little geo- graphic structuring is seen in C. onyx over 132 km of the southern Californian coast. C. onyx was the only Crepidula species found in Mission Bay during our study and there was no observational or genetic reason to suspect the presence of a second cryptic species. The phenogram ( Woodruff et al., 1986: Fig. 1) comparing C. onyx with C. adunca, a species that replaces it on the central coast of California, provides no support for the hypothesis that these two taxa were confused in our samples. Most Crepidula species that have been compared have interspecific Nei's genetic dis- tances in the range D ¼ 0.4-0.9 and the minimum reported ...
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... values are high but are not without precedence in nature (Endler, 1986). Similar high values when they have been reported are usually associated with a single locus and have been documented in well-studied cases involving Ldh in the fish Fundulus and Pgi in the butterfly Colias (Mitton, 1997). Nevertheless, the levels of selection implied here, and their breadth of action across the genome, are extraordinary, and we have little confidence in our default conclusion. ...
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Citations
... Temporal samples were tested for conformance to Hardy-Weinberg equilibrium (HWE) and linkage disequilibrium (LD) expectations using Genepop v4.3 (Rousset 2008). Heterozygote deficits are common in many mollusks (Li et al. 2003;Plutchak et al. 2006), especially dreissenid mussels (Marsden et al. 1995;Wilson et al. 1999;Elderkin et al. 2001;Astanei et al. 2005;Therriault et al. 2005;Gosling et al. 2008;Imo et al. 2010;Feldheim et al. 2011;Marescaux et al. 2016;Mallez and McCartney 2017;Lindsay et al. 2018), which may be attributed to the Wahlund effect (Marescaux et al. 2016). Therefore, we used FreeNA (Chapuis and Estoup 2007) to calculate and correct for null alleles and heterozygote deficiency in our population samples. ...
Genetic compositions and comparative diversity of zebra (Dreissena polymorpha) and quagga (D. rostriformis) mussel populations are compared across their three decade-long histories as invasive species in the Hudson River and Lake Erie of North America. We analyze 15 nuclear DNA microsatellite loci for the zebra mussel and 10 for the quagga mussel. Results indicate that the Hudson River and Lake Erie zebra mussel populations slightly diverge in genetic compositions, and possess similar overall genetic diversity levels. The allelic composition of the Hudson River zebra mussel population significantly changed during the middle time period (2003) analyzed, suggesting genetic replacement. Yet, its overall levels of genetic diversity levels have stayed similar. In contrast, the Hudson River’s quagga mussel population has remained genetically consistent over time in both composition and diversity. Lake Erie’s zebra mussel population underwent slight change in allelic composition and increased in genetic diversity from the earliest timepoint, suggesting allelic
supplementation from newly arriving propagules. In contrast, Lake Erie’s quagga mussel population has remained genetically consistent over time. The genetic composition of Lake Erie zebra mussel veliger larvae sampled in 2016 differed from its adult samples, attributable to gene flow from other areas and genetic admixture. Overall findings indicate that invasive populations may undergo significant genetic divergence or remain consistent over time, whose patterns may
differ across their ranges and between related species. The population dynamics underlying their invasional successes thus may be complex.
... Selection against heterozygotes cannot be demonstrated from our results, although it is important to stress that positive selection is suggested on the Pn 3.6 locus using LOSITAN software (data not included). In fact, this locus, Pn 3.6, also shows the lowest value of observed heterozygotes in all adult and juvenile sampled localities with respect to the other loci studied, which could imply a selection against heterozygotes (Borsa, Zainuri, & Delay, 1991;Brownlow et al., 2008;Plutchak, Simmons, & Woodruff, 2006;Toro & Vergara, 1995). That selection means that the heterozygotes have a lower fitness than homozygotes; this fact could affect the adaptation potential of P. nobilis and its spatial genetic variation patterns. ...
• Pinna nobilis is an endemic bivalve of the Mediterranean Sea, and a vulnerable species registered as endangered and protected under the European Council Directive 92/43/EEC and Barcelona Convention.
• In early autumn 2016, a mass mortality event impacted P. nobilis populations in the south‐western Mediterranean Sea, including the Balearic Islands. At the time of this study, P. nobilis still maintained high population densities along the Balearic coasts (Western Mediterranean).
• This study evaluated the connectivity of P. nobilis post‐larvae and adults in seagrass habitats around the Balearic Islands and identified its source and sink populations. These objectives were reached through a multidisciplinary approach including population genetics (10 microsatellites) and hydrodynamic modelling.
• High genetic diversity was found and significant genetic differentiation (inferred by fixation index FST) was detected between post‐larvae samples, but not between adult populations. Significant genic and genotypic differentiation was recorded for adults and post‐larvae.
• This pattern was confirmed by correspondence analysis using allele frequencies. The genetic connectivity pattern was consistent with marine currents and dispersal models.
• This work not only improves knowledge of the P. nobilis gene pool in south‐west Mediterranean populations and their connectivity patterns, but is also crucial to help evaluate the possibility of recovery from source populations and the possibility of restocking programmes, as well as provide a solid base to establish effective marine reserve networks.
... The uptake and bioaccumulation of BDE-47 into the larvae, juveniles and adults of C. onyx via dietary intake and maternal transfer were also evaluated. C. onyx has a biphasic life cycle, well-studied embryonic development (Henry et al., 2010) and a wide distribution along the Pacific coast of North and South America, China, Japan and Hong Kong (Plutchak et al., 2006). Crepidula spp. ...
Polybrominated diphenyl ethers have become ubiquitous in the environment and elevated concentrations have often been found in marine organisms. Using the gastropod Crepidula onyx as a study model, this multigenerational study sets out to test the hypotheses that 1) parental dietary exposure to environmentally realistic levels of 2,2',4,4'-tetrabrominated diphenyl ether (BDE-47) would lead to transgenerational impairments on fitness traits of marine invertebrates, and 2) the organisms might develop adaptation/acclimation after exposure for one or more generations. F0 generation of C. onyx was fed with the dinoflagellate Isochrysis galbana encapsulated with two concentrations of BDE-47 (1.78 and 16.0 ng million cells-1, respectively), and half of the F1 offspring from the higher concentration treatment was returned to control condition (transgenerational group), while the other half received BDE-47 treatment continuously (continuous treatment group). Bioaccumulation and maternal transfer of BDE-47 were evident in all life stages of the F0 generation and in F1 eggs, respectively. Exposure to BDE-47 reduced fecundity, delayed sexual maturity, and impeded embryonic development in F0 to F2. In particular, developmental toxicity of F2 embryos was apparent in the transgenerational group, but not in the continuous treatment group, even when BDE-47 was not detected in the F2 embryos nor in their mothers and they have never been exposed to the chemical. This study also suggested that the offspring might have developed adaptation/acclimation to the exposure of BDE-47 within two generations of exposure, and that the physiological alterations associated with acclimation/adaptation might have hindered the normal larval development under a stress free condition. These findings highlighted the need for long-term multigenerational studies in the ecological risk assessment of chemicals alike.
... Carlsson (2008) investigated the effect of null alleles and concluded that microsatellite loci affected by null alleles would probably not alter the overall outcome of population analyses and could, therefore, be included in studies. Furthermore, the presence of null alleles appears to be fairly common in sea cucumbers and other marine invertebrates ( Addison and Hart 2005;Plutchak et al. 2006;Dailianis et al. 2011;Kang et al. 2011). However, the eight loci prone to null alleles (Lca20, Lca49, Lca54, Lca59, Lca40, Lca4, Lca48 and Lca17) were used with caution and where possible tests were also performed using the adjusted genotypes to validate outcomes. ...
... To account for any effects of null alleles, DAPC analysis was used because it describes variation among subpopulations only and does not rely on a particular population-genetic model; thus, it is free of assumptions about HWE or LD (Jombart et al. 2010). Furthermore, the occurrence of null alleles is quite common in sea cucumbers and other marine invertebrates and has been reported in the sea cucumber Stichopus japonicus (Chang et al. 2009), the Pacific oyster Crassostrea gigas (Launey and Hedgecock 2001) the snail Crepidula onyx (Plutchak et al. 2006), the coral Pocillopora damicornis (Whitaker 2006) and the starfish Acanthaster planci (Yasuda et al. 2009). Although unlikely, biological causation for the deficits of heterozygotes cannot be ruled out. ...
The development of a sandfish (Holothuria scabra) mariculture industry within Papua New Guinea (PNG) is of great socio-economic importance. However, the lack of knowledge surrounding the current population genetic structure throughout the region has raised concern about the genetic impacts of hatchery-augmented sea ranching on already diminished wild populations. The present study evaluated the current population genetic structure of sandfish within PNG, and more broadly across northern Australia, to inform sustainable mariculture practices and provide baseline genetic data within these regions. Microsatellite-based population genetic analyses were used to determine the genetic diversity within subpopulations. This analysis found that although microsatellite loci varied widely in the number of alleles (3–28), the overall allelic diversity was similar among all populations sampled. The level of genetic substructuring among all populations sampled was low, although significant (FST=0.037, P=0.000). Most of these differences were driven by distinctness of the Australian populations from those in PNG, whereby results indicated that PNG populations exhibited a panmictic stock structure. No distinct patterns of genetic isolation by distance were detected among the populations examined. Information obtained from the present study will improve the management of restocking programs and support a sustainable future for the PNG sandfish mariculture industry.
... The overall levels of observed heterozygosity across all populations were lower than expected (Table 1). However, heterozygote deficits have been well documented in P. margaritifera and P. maxima (Arnaud-Haond et al., 2008;Durand and Blanc, 1988;Durand et al., 1993;Lind et al., 2009), as well as other marine molluscs (Brownlow et al., 2008;Hedgecock et al., 2004;Miller et al., 2013;Peñaloza et al., 2014;Plutchak et al., 2006). A number of explanations have been proposed for this observation, including inbreeding effects, null alleles, aneuploidy, Wahlund effects (reduced heterozygosity caused by sub-population structuring) and indirect or direct natural selection acting on marker loci (Beaumont, 1991;Peñaloza et al., 2014;Zouros and Foltz, 1984). ...
... Arnaud-Haond et al., 2008), inbreeding alone is unlikely to account for the absence of heterozygotes as other signatures such as reductions in N e and correlated trends in multilocus metrics (Table 1; IR, SH, HL) were absent. It is equally unlikely that the inflated F is values result from a Wahlund effect or aneuploidy, given the panmictic population structure (NetView P network) and high levels of gene flow detected, and that to date no natural case of haploidy has been documented in the Mollusca (Plutchak et al., 2006). ...
Population genomic investigations on highly dispersive marine organisms typically require thousands of
genome-wide SNP loci to resolve fine-scale population structure and detect signatures of selection. This information is important for species conservation efforts and stockmanagement in bothwild and captive populations, as well as genome mapping and genome wide association studies. Double digest Restriction site-Associated DNA Sequencing (ddRADseq) is a recent tool for delivering genome wide SNPs for non-model organisms. However, its application to marine invertebrate taxa has been limited, particularly given the complex and highly repetitive nature of many of these organisms' genomes. This study develops and evaluates an optimised ddRADseq technique together with associated analyses for generating genome-wide SNP data, and performs population genomic analyses to inform aquaculture and fishery management of a marine bivalve, the black-lip pearl oyster Pinctada margaritifera. A total of 5243 high-quality genome-wide SNP markers were detected, and used to assess population structure, genome diversity, detect Fst outliers and perform association testing in 156 individuals belonging to three wild and one hatchery produced populations from the Fiji Islands. Shallow but significant population structure was revealed among all wild populations (average pairwise Fst =0.046) when visualised with DAPC and an individual network analysis (NetView P),with clear evidence of a genetic bottleneck in the hatchery population (NeLD=6.1), compared to wild populations (NeLD N 192.5). Fst outlier detection revealed 42–62 highly differentiated SNPs (p b 0.02), while case–control association discovered up to 152 SNPs (p b 0.001). Both analyseswere able to successfully differentiate individuals between the orange and black tissue colour morphotypes characteristic of this species. BLAST searches revealed that five of these SNPs were associated with a melanin biosynthesis pathway, demonstrating their biological relevance. This study has produced highly informative SNP and population genomic data in P. margaritifera, and using the same approach promises to be of substantial value to a range of other non-model, broadcast-spawning or marine invertebrate taxa.
... 2.2.3 (Van Oosterhout et al. 2004) found significant evidence of null alleles in the 11 loci out of HWE but no evidence of scoring errors or large allele dropout. Deviation from HWE due to null alleles appears to be fairly common in sea cucumbers and other marine invertebrates (see Addison and Hart 2005;Plutchak et al. 2006;Whitaker 2006;Chang et al. 2009;Yasuda et al. 2009;Dailianis et al. 2011;Kang et al. 2011). Furthermore, the 18 loci were examined for Mendelian transmission of alleles between parents (n = 17) and offspring (n = 50) by comparing genetic data with known pedigree data in CERVUS 3.0.3. ...
We isolated 18 new, polymorphic, microsatellite markers from Holothuria scabra, a commercially important species of sea cucumber found throughout the Asia-Pacific region. Next-generation sequencing was used to identify 206 unique loci for which primers were designed. Of these unique loci, we trialled 65 primer pairs in the target species, and 48 (74%) amplified a product of the expected size. Eighteen loci were found to be polymorphic and reliable, and were screened for variation in 50 individuals, from a single population from Croker Island, Northern Territory, Australia. Observed heterozygosity ranged from 0.00 to 0.96 (mean = 0.46) and the number of alleles per locus from 2 to 28 (mean = 9.61). These loci will be useful for the investigation of population structure and mating systems in H. scabra and may also be of use in other holothurian species.
... Over two decades, multi-locus heterozygosity deficiency relative to the departures from HWE has been the subject of extensive work dealing with population genetics of diverse bivalves and gastropods. [21][22][23][24][25] As for bivalves, this phenomenon is relatively common in natural populations, and some hypotheses have been accounted for unexpected heterozygosity deficiency, such as allele scoring bias, presence of null alleles, inbreeding, spatial and temporal Wahlund effects (i.e. reduction of heterozygosity in a population caused by subpopulation structure), age effects and direct natural selection on the marker loci. ...
Allozyme variation of the littleneck clam Ruditapes philippinarum was evaluated in four samples from Nameishi and Matsuo in the Ariake Sea, Ryugatake and Ushibuka in the Shiranui Sea off Kyushu Island, Japan, and in one sample from Jinzhou, China, in the Bohai Sea. A Ruditapes bruguieri sample imported from the Korean Bay off Nampo, North Korea was also studied. Among the R. philippinarum samples, heterozygosity varied from 0.265 to 0.301 and F
is estimates indicated significant homozygosity excess in 15 of 40 loci analyzed. Deviations from Hardy-Weinberg equilibrium were significant in all samples (P<0.05). Pairwise F
ST estimates indicate that genetic differences between the Chinese and Japanese samples were very low, but significantly different from zero. Mixture proportions with 95% confidence intervals of Chinese R. philippinarum in Nameishi and Matsuo were estimated at 0.4098 [0.2512, 0.5705] and 0.4899 [0.3262, 0.6540], respectively. However, genetic invasion of stocked Chinese R. philippinarum into wild populations in the Ariake Sea remains uncertain due to the low precision of the estimates caused by the high similarity of allele frequencies between Jinzhou and the Ariake Sea.
... Studies of the mechanisms behind heterozygote deficiency may be of special interest in molluscs, since puzzling heterozygote deficiency in allozyme loci has been reported in many bivalves and gastropods (Zouros & Foltz, 1984;Raymond et al., 1997;Andrade, Medeiros & Solferini, 2005;Plutchak, Simmons & Woodruff, 2006). The explanations offered to account for this phenomenon involve biological characteristics of the species (inbreeding, spatial and temporal population structure, selection) as well as possible genotyping errors (misscoring and null alleles). ...
Microsatellite DNA is widely used as population genetic marker, but the cost of using microsatellites is high, as they usually
need to be developed and optimized for each species separately. Cross-species amplification of microsatellites is therefore
commonly applied to bring down the cost, but it can also involve genotyping errors. We studied cross-species amplification
of microsatellites in four species of the Atlantic group of Littorina (Neritrema): L. saxatilis (Olivi, 1792), L. obtusata (Linnaeus, 1758), L. fabalis (Turton, 1825) and L. arcana Hannaford Ellis, 1978 to investigate whether markers originally developed for a more distantly related Pacific species [L. subrotundata (Carpenter, 1864)] suffered from more amplification problems than markers developed for one of the species in the Atlantic
group (L. saxatilis). We also compared variation in amplification success among the species and among different regions in the NE Atlantic. Approximately
half of the 12 primers developed for L. subrotundata and the seven primers developed for L. saxatilis were successfully amplified in other species of the subgenus. The success was dependent on phylogenetic distance among species
within the subgenus. On the other hand, the variation in performance of the loci between geographically remote populations
of the same species was as high as variation among the species. In earlier studies statistical analyses indicated that several
loci showed a heterozygote deficiency due to null alleles. The presence of null alleles was confirmed by a segregation analysis
of the microsatellite loci in eight half-sib families of L. saxatilis.
... There was an overall deficiency of heterozygotes at all sites and these deficits were significant in 14 of 40 cases (Table 1). Heterozygote deficits are a common occurrence in marine bivalves (see Plutchak, Simmons & Woodruff, 2006 for comprehensive list of references) and have frequently been reported in D. polymorpha (Boileau & Hebert, 1993;Marsden et al., 1995;Soroka et al., 1997;Lewis et al., 2000;Elderkin et al., 2001). Several factors, such as inbreeding, the Wahlund effect, genotyping bias, the presence of null alleles or selection, could account for the observed heterozygote deficits. ...
1. The recent arrival and explosive spread of the zebra mussel, Dreissena polymorpha (Pallas), in Ireland provided a rare opportunity to study the population genetics of an invasive species.
2. Eight polymorphic allozyme loci (ACO-1, ACO-2, EST-D, GPI, IDH-2, MDH, OPDH and PGM) were used to investigate genetic diversity and population structure in five Irish populations, and the results were compared with those from a previous microsatellite study on the same samples.
3. The mean number of alleles per locus (2.7 ± 0.1) was similar to the mean for the same loci in European populations, suggesting that Irish founder populations were large and/or multiple colonization events took place after foundation. A deficiency of heterozygotes was observed in all populations, but was uneven across loci.
4. Pairwise comparisons, using Fisher’s exact tests and FST values, revealed significant genetic differentiation among populations. The overall multilocus FST estimate was 0.118 ± 0.045, which contrasted with an estimate of 0.015 ± 0.007 from five microsatellite loci on the same samples in a previous study.
5. Assuming that microsatellites can be used as a neutral baseline, the discordant results from allozymes and microsatellites suggest that selection may be acting on some allozyme loci, specifically ACO-1, ACO-2, IDH-2 and MDH, which contributed most to the significant differentiation between samples.
... Signi¢cant deviations from H^WE with heterozygote de¢ciencies were found in six populations. Heterozygote de¢ciencies are common in marine invertebrates (Hare, Karl & Avise 1996) and could indicate population mixing (Wahlund e¡ect) or a number of actual or artefactual factors (Plutchak, Simmons & Woodru¡ 2006). Population mixing is particularly possible during juvenile stages when larvae from di¡erent populations can meet in shallow waters before joining adult populations in o¡shore waters during the reproductive season. ...
Ten populations of Penaeus kerathurus (Forskl), a prawn of high commercial value, were sampled from the eastern and western Mediterranean coastal waters of Tunisia and screened electrophoretically for genetic variation at 13 allozyme loci. Four among the six polymorphic loci were out of Hardy–Weinberg equilibrium (H–WE) in at least one population. In the same way, the multilocus test showed deviation from H–WE in six populations. These populations showed heterozygote deficiency whereas the average heterozygosity for the four remaining ones is quite similar to the expected levels. Genetic variability was low. The number of alleles per locus ranged from 1.2 to 1.5 (average=1.3), and the observed heterozygosity varied between 0.010 and 0.048 (average=0.021). Significant population differentiation (FST=0.076, P<0.05) in the total data set reflected the differentiation of the two populations, which were at the margins of the range sampled, from all the others (Pairwise FST values ranged from 0.035 to 0.208). Although there was no significant differentiation among the other populations (pairwise FST values ranged from −0.006 to 0.201, P>0.05). Our data suggest a population structure consistent with separation by Mediterranean Sea basins that might reflect different local biogeographical zones.
