The developmental genetics of dextrality and sinistrality in the gastropodLymnaea peregra

Abstract

The genetics of body asymmetry inLymnaea peregra follows a maternal mode of inheritance involving a single locus with dextrality being dominant to sinistrality. Maternal inheritance implies that all members of a brood have the same phenotype, however, some broods contain a few individuals of opposite coil. One purpose of this paper is to explain the origin of these anomalous individuals. Genetic analyses of sinistral broods with a few dextral individuals have led to the development of a cross-over model, with the anomalous dextrals originating as a consequence of crossing over either during meiosis or mitosis in the female germ line. The crossover either reconstitutes the dextral gene from previously dissociated parts, or creates a dextral gene by means of a position effect. The probability of a crossover event depends upon the appropriate combination of complementary sinistral chromosomes. Each crossover event has the potential of creating a unique dextral gene. Genetic analyses of dextral broods containing a few sinistral individuals have demonstrated that different dextral genes vary in penetrance.The dextral gene produces a product during oogenesis which influences the pattern of cleavage in the embryo; this cleavage pattern is translated into the appropriate body asymmetry. The other purpose of this paper is to provide an assay for this gene product. Cytoplasm from dextral eggs injected into uncleaved sinistral eggs causes these eggs to cleave in a dextral pattern. Cytoplasm from sinistral eggs has no effect on the cleavage pattern of dextral eggs. While the dextral gene product is made during oogenesis, it does not function in controlling cleavage until just before this process begins.

What determines direction of asymmetry: genes, environment or chance?

“…Species that normally have dextrally coiled shells exhibit dextral cleavage at the eight-cell stage. However, sinistral cleavage at the eight-cell stage, owing either to natural genetic variation [32,85] or to experimental manipulation of blastomere arrangements [45,75], yields a snail with a sinistrally coiled shell. In addition, some polychaete embryos exhibit reversed chirality in up to 10% of single broods (table 3).…”

Far from solved: A perspective on what we know about early mechanisms of left–right asymmetry

“…Other important questions remain: What is the nature of the maternal chirality-determining factor in snails (Freeman and Lundelius, 1982)? The data suggest strongly that the cytoskeleton is crucial in determining very early events of asymmetry but what is the role of the factor that has been demonstrated in cytoplasm transfer experiments but not molecularly identified?…”

Coil and shape in Partula suturalis: the rules of form revisited

“…When cytoplasm from dextral L. peregra embryos was injected into sinistral embryos, some of the receiving eggs then developed dextrally (Freeman and Lundelius, 1982). Unfortunately this work was not followed up.…”

“…It is still a staple item in textbooks (Gilbert, 2006), and continues to mold current thinking (Gurdon, 2005;Wood, 2005;Levin and Palmer, 2007), yet progress in understanding the establishment of molluscan asymmetry is limited to a few key papers since 1940 (Freeman and Lundelius, 1982;Shibazaki et al, 2004;Grande and Patel, 2008). This is unfortunate because, although the vast majority of molluscan species are dextral, sinistrals are found not only as isolated individuals, but also as whole populations, species and even families (Asami et al, 1998).…”