Abstract
In the present work we report evidence compatible with a maternal effect allele affecting left-right development and functional lateralization in vertebrates. Our study demonstrates that the increased frequency of reversed brain asymmetries in a zebrafish line isolated through a behavioral assay is due to selection of mother-of-snow-white (msw), a maternal effect allele involved in early stages of left-right development in zebrafish. msw homozygous females could be identified by screening of their progeny for the position of the parapineal organ because in about 50% of their offspring we found an altered, either bilateral or right-sided, expression of lefty1 and spaw. Deeper investigations at earlier stages of development revealed that msw is involved in the specification and differentiation of precursors of the Kupffer's vesicle, a structure homologous to the mammalian node. To test the hypothesis that msw, by controlling Kupffer's vesicle morphogenesis, controls lateralized behaviors related to diencephalic asymmetries, we analyzed left- and right-parapineal offspring in a “viewing test”. As a result, left- and right-parapineal individuals showed opposite and complementary eye preference when scrutinizing a model predator, and a different degree of lateralization when scrutinizing a virtual companion. As maternal effect genes are expected to evolve more rapidly when compared to zygotic ones, our results highlight the driving force of maternal effect alleles in the evolution of vertebrates behaviors.
Highlights
During the evolution of animal body plans, symmetry has been broken at least three times, possibly for purposes linked to feeding and escape behaviors
We showed that selection for right-eye preference in inspecting a social stimulus increased the frequency of individuals with reversed epithalamic asymmetries; in the TLRE strain, after five generation of artificial selection the frequency of embryos with reversed asymmetry in the position of the parapineal organ increased from 12.5% of the wild type stock (TL) to 35.8% [21]
In the present work we report the evidence of a naturally occurring semi-dominant maternal effect trait affecting left-right development and functional lateralization in zebrafish
Summary
During the evolution of animal body plans, symmetry has been broken at least three times, possibly for purposes linked to feeding and escape behaviors. In the vertebrate embryo the event responsible for breaking initial symmetry occurs during late gastrulation at the posterior end of the notochord in an evolutionarily conserved transient ciliated structure: the mammalian node, the gastrocoel roof plate in Xenopus; the Kupffer’s vesicle in zebrafish [5,6] Cilia of this structure displays a rotating beating movement that generate a leftward flow of extracellular fluid which triggers the asymmetrical transcription of Nodal genes on the left lateral plate mesoderm [7,8,9]. Disturbance or absence of nodal leftward flow results in laterality defects and randomization of left-right asymmetries in vertebrates and situs inversus in humans [12,13,14,15,16] It has been reported evidence of nodal and Pitx orthologues expression in two species of snails with opposite body handedness and direction of shell coiling. From previous studies it is known that in snails, body handedness is controlled by a maternal effect trait that determines the direction of shell coiling in the offspring [18,19,20]
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