Physiological bases of genetically determined variation in growth of marine invertebrate larvae: A study of growth heterosis in the bivalve Crassostrea gigas

Pace, Douglas A.; Marsh, Adam G.; Leong, Philip H. W.; Green, Allison J.; Hedgecock, Dennis; Manahan, Donal T.

doi:10.1016/j.jembe.2006.03.005

Cited by 86 publications

(63 citation statements)

References 76 publications

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“…Potence values for the two reciprocal hybrids are much greater than 1.0 (h 35 ϭ 4.56, P Ͻ 0.0001; h 53 ϭ 7.93, P Ͻ 0.0001); hybrid 53 is significantly larger than hybrid 35 (P ϭ 0.0012) and inbred family 33 is larger, although not significantly so, than inbred family 55 (P ϭ 0.054). Clearly, our experimental material exhibits classical hybrid vigor or growth heterosis, as observed in previous crosses among inbred lines (15,17,18).…”

supporting

confidence: 52%

“…These patterns of expression may be related to physiological differences that have been observed between fastand slow-growing oyster larvae with different genotypes. Pace et al (18) showed that the physiological bases of growth heterosis in larvae were enhanced feeding rate and metabolic efficiency likely realized through mechanisms of protein synthesis and degradation (turnover). For adult bivalves, Hawkins et al (19) showed that much of the difference in resting metabolic rates between fast-and slow-growing mussels could be ascribed to differences in whole-body protein turnover.…”

Section: Discussionmentioning

confidence: 99%

“…Physiological causes of heterosis have received less attention than genetic causes (10), but classical methods for quantifying energy and nutrient budgets are advancing understanding of the physiological underpinnings of growth heterosis in bivalves. Both larval and adult hybrid oysters have higher feeding rates and efficiencies than their inbred counterparts (17,18). A large proportion of growth efficiency is achieved by lower rates of protein turnover in hybrids or more highly heterozygous individuals (19).…”

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confidence: 99%

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Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )

Hedgecock

Lin²,

Decola³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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123

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Compared with understanding of biological shape and form, knowledge is sparse regarding what regulates growth and body size of a species. For example, the genetic and physiological causes of heterosis (hybrid vigor) have remained elusive for nearly a century. Here, we investigate gene-expression patterns underlying growth heterosis in the Pacific oyster (Crassostrea gigas) in two partially inbred (f ‫؍‬ 0.375) and two hybrid larval populations produced by a reciprocal cross between the two inbred families. We cloned cDNA and generated 4.5 M sequence tags with massively parallel signature sequencing. The sequences contain 23,274 distinct signatures that are expressed at statistically nonzero levels and show a highly positively skewed distribution with median and modal counts of 9.25 million and 3 transcripts per million, respectively. For nearly half of these signatures, expression level depends on genotype and is predominantly nonadditive (hybrids deviate from the inbred average). Statistical contrasts suggest Ϸ350 candidate genes for growth heterosis that exhibit concordant nonadditive expression in reciprocal hybrids; this represents only Ϸ1.5% of the >20,000 transcripts. Patterns of gene expression, which include dominance for low expression and even underdominance of expression, are more complex than predicted from classical dominant or overdominant explanations of heterosis. Preliminary identification of ribosomal proteins among candidate genes supports the suggestion from previous studies that efficiency of protein metabolism plays a role in growth heterosis.MPSS ͉ nonadditive expression ͉ factorial cross of partially inbred lines ͉ potence ͉ protein metabolism W hole-genome sequencing has yielded rich insights into the number of genes required to make complex eukaryotic animals (1-4). Surprisingly few genes, however, can effect major changes in body design and shape. For example, elaboration and mutation of a fairly small number of developmentally important regulatory genes, such as the Hox gene cluster, appear to have driven the evolution of the major metazoan body plans (5). Profound changes in shape or morphology, underlying adaptive differences among closely related species, also can be caused by mutations in a very few genes (6-8).Compared with our growing understanding of the evolution of biological shape and form, our understanding of what regulates body size and the rates and efficiencies of physiological functions is much less developed. For example, the genetic and physiological causes of heterosis (hybrid vigor) and its converse, inbreeding depression, have remained elusive for nearly a century, despite the economic and scientific significance of these phenomena (9-12). Major genetic explanations for heterosis are overdominance, the superiority of heterozygotes at genes affecting fitness or economic traits, dominance, the masking, in hybrids, of deleterious recessive mutations by dominant alleles inherited from one or the other inbred parent, and epistasis, the interaction of alleles at differe...

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supporting

confidence: 52%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )

Hedgecock

Lin²,

Decola³

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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123

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“…Mothers control the development mode of their offspring via egg energy content, and determine whether embryos have a period of benthic development in protective capsules (Strathmann, 1985(Strathmann, , 1990(Strathmann, , 1995Levin and Bridges, 1995;Moore and Manahan, 2007). Larval genotype can affect metabolic efficiency and pelagic period (Levin et al, 1991;Pace et al, 2006;Hedgecock et al, 2007;Pace and Manahan, 2007), as well as habitat choice behavior (Toonen and Pawlik, 2001a). There is thus considerable potential for adaptive variation in traits related to larval size, hatching, dispersal, and habitat selection in marine life histories.…”

Section: Introductionmentioning

confidence: 99%

Not My “Type”: Larval Dispersal Dimorphisms and Bet-Hedging in Opisthobranch Life Histories

Krug

2009

The Biological Bulletin

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Abstract. When conditions fluctuate unpredictably, selection may favor bet-hedging strategies that vary offspring characteristics to avoid reproductive wipe-outs in bad seasons. For many marine gastropods, the dispersal potential of offspring reflects both maternal effects (egg size, egg mass properties) and larval traits (development rate, habitat choice). I present data for eight sea slugs in the genus Elysia (Opisthobranchia: Sacoglossa), highlighting potentially adaptive variation in traits like offspring size, timing of metamorphosis, hatching behavior, and settlement response. Elysia zuleicae produced both planktotrophic and lecithotrophic larvae, a true case of poecilogony. Both intracapsular and post-hatching metamorphosis occurred among clutches of "Boselia" marcusi, E. cornigera, and E. crispata, a dispersal dimorphism often misinterpreted as poecilogony. Egg masses of E. tuca hatched for up to 16 days but larvae settled only on the adult host alga Halimeda, whereas most larvae of E. papillosa spontaneously metamorphosed 5-7 days after hatching. Investment in extracapsular yolk may allow mothers to increase larval size relative to egg size and vary offspring size within and among clutches. Flexible strategies of larval dispersal and offspring provisioning in Elysia spp. may represent adaptations to the patchy habitat of these specialized herbivores, highlighting the evolutionary importance of variation in a range of life-history traits.

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“…Growth of bivalves seems to be related to the genetic conformation of the individual (Meyer & Manahan, 2010). High levels of homozygosity due to inbreeding can significantly reduce growth rate (Beaumont & Abdul-Martin, 1994) and, conversely, high degrees of heterozygosity (Bayne, 1999;Crnokrak & Barrett;Pace et al, 2006) may enhance growth rate. Hybridization should increase the heterozygosity of individuals, which may in part explain the higher growth observed in hybrid larval cultures in the present study.…”

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confidence: 99%

Production and performance of larvae and spat of pure and hybrid species of Mytilus chilensis and M. galloprovincialis from laboratory crosses

Toro

Oyarzún

Peñaloza

et al. 2012

lajar

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ABSTRACT. Adult specimens of M. galloprovincialis from Concepción Bay and M. chilensis from Yaldad Bay, Chile, were transferred to the laboratory to produce crosses of "pure" and "hybrid" species in order to evaluate early larval development and growth. These variables are important for understanding the dynamics of these two mussel species in this potential hybrid zone where they occur sympatrically. The study showed that fertilization occurred in all crosses and significant differences were not detected between pure lines and hybrids in terms of the percentage of eggs that developed into larvae. Hybrid larvae and spat from both reciprocal crosses grew significantly more than those from pure lines, although valve length values were within the ranges reported in the literature. Keywords: Mytilus chilensis, Mytilus galloprovincialis, larval development, hybrids, Chile. Producción y comportamiento de larvas de especies puras e híbridas entreMytilus chilensis y Mytilus galloprovincialis obtenidas en laboratorio RESUMEN. Ejemplares adultos de M. galloprovincialis de la bahía de Concepción y de M. chilensis de la bahía de Yaldad, Chile, se trasladaron al laboratorio para realizar cruzamientos puros de cada especie e híbridos, para evaluar el desarrollo larval temprano y su crecimiento. Estas variables son importantes para entender la dinámica de estas dos especies de mitílidos en esta potencial zona híbrida donde se encuentran en forma simpátrica. El estudio mostró que la fertilización ocurrió en todos los cruzamientos y no se detectó diferencias significativas entre líneas puras e híbridas en el porcentaje de huevos que se desarrollaron a larvas. Las larvas y juveniles híbridos de ambos cruzamientos recíprocos crecieron significativamente más que las larvas de los cruzamientos de especies puras, aunque los valores de longitud de la valva están dentro de los rangos reportados en la bibliografía. There is no evidence in the literature for the presence of unfit hybrid recombinants within Mytilus hybrid zones (Comesaña et al., 1999;Toro et al., 2002;Beaumont et al., 2004;Westfall & Gardner, 2010;Dias et al., 2011). As discussed by Comesaña et al. (1999), the degree of natural hybridization is generally higher in the Mytilus edulis-M. galloprovincialis hybrid zone in Europe than in the M. edulis-M. trossulus hybrid zone on the east coast of north America. According to Harrison (1993) the more genetically divergent the parental types, the lower will be the fitness of the hybrids produced. This difference in natural hybridization in these two mussel hybrid zones implies that M. edulis and M. galloprovincialis are more closely related (Gardner, 1994) than are M. edulis and M. trossulus (Rawson et al., 1996). This has been corroborated by successful interbreeding between M. edulis and M. galloprovincialis, the

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Physiological bases of genetically determined variation in growth of marine invertebrate larvae: A study of growth heterosis in the bivalve Crassostrea gigas

Cited by 86 publications

References 76 publications

Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )

Transcriptomic analysis of growth heterosis in larval Pacific oysters ( Crassostrea gigas )

Not My “Type”: Larval Dispersal Dimorphisms and Bet-Hedging in Opisthobranch Life Histories

Production and performance of larvae and spat of pure and hybrid species of Mytilus chilensis and M. galloprovincialis from laboratory crosses

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