Natural allelic variations of xenobiotic-metabolizing enzymes affect sexual dimorphism inOryzias latipes

Abstract

Sexual dimorphisms, which are phenotypic differences between males and females, are driven by sexual selection. Interestingly, sexually selected traits show geographical variations within species despite strong directional selective pressures. This paradox has eluded many evolutionary biologists for some time, and several models have been proposed (e.g. 'indicator model' and 'trade-off model'). However, disentangling which of these theories explains empirical patterns remains difficult, because genetic polymorphisms that cause variation in sexual differences are still unknown. In this study, we show that polymorphisms in cytochrome P450 (CYP) 1B1, which encodes a xenobiotic-metabolizing enzyme, are associated with geographical differences in sexual dimorphism in the anal fin morphology of medaka fish (Oryzias latipes). Biochemical assays and genetic cross experiments show that high-and low-activity CYP1B1 alleles enhanced and declined sex differences in anal fin shapes, respectively. Behavioural and phylogenetic analyses suggest maintenance of the high-activity allele by sexual selection, whereas the low-activity allele possibly has experienced positive selection due to by-product effects of CYP1B1 in inferred ancestral populations. The present data can elucidate evolutionary mechanisms behind genetic variations in sexual dimorphism and indicate trade-off interactions between two distinct mechanisms acting on the two alleles with pleiotropic effects of xenobiotic-metabolizing enzymes.

Variation in the ontogeny of sex steroid levels between latitudinal populations of the medaka

“…Interestingly, many genes involved in steroid metabolism, such as cytochrome P450 ( CYP ) genes, were found near the QTL [ 15 ], suggesting that variation in the size-specific expression of these steroid metabolism genes results in the interpopulation variation in sexual dimorphism in fin lengths. It has also been shown that polymorphisms in CYP genes are associated with variation in sexual dimorphism in the anal fin morphology between Japanese and Korean populations; high-activity alleles enhance sexual difference in anal fin shapes [ 21 ], supporting that CYP genes are responsible for the interpopulation variation in the ontogeny of sex steroid levels and resultant variation in fin lengths.…”

“…For example, androgens are known to increase the expression of male-specific appendages or ornaments but they also promote courtship behaviors and territorial aggressions [ 41 – 44 ]. In support of this, it has been demonstrated that male medaka from lower-latitude populations fight each other more frequently than do males from higher-latitude populations and that lower-latitude males also tend to court females more frequently [ 21 ]. Theoretically, such male-specific appendages and mating behaviors are thought to evolve through sexual selection [ 2 , 45 ].…”

“…Populations inhabiting contrasting environments exhibit geographical variation in sexual dimorphism in guppies [ 18 ] and sticklebacks [ 19 , 20 ]. In the medaka also, geographic variation in the magnitudes of sexual dimorphisms in fin morphologies has been reported [ 14 , 21 , 22 ]. Generally, the anal and dorsal fins of mature males in low-latitude populations are longer than those of higher-latitude males, resulting in greater sexual dimorphism in southern than in northern populations [ 14 , 22 ].…”

DNA methylation site loss for plasticity-led novel trait genetic fixation

“…The details are in the supplementary table S1. To explore the genetically-fixed gut length in medaka populations, we sampled 400 individuals from 40 wild-derived laboratory stocks that originated from wild populations, which had been maintained in a constant environment at an outdoor breeding facility, the University of Tokyo 11,23 Yongcheon, Maegok, Bugang, Sacheon, Shanghai. The subgroup names in parentheses are defined in our prior study 11 .…”

An Approach to Elucidate NBS1 Function in DNA Repair Using Frequent Nonsynonymous Polymorphism in Wild Medaka (Oryzias latipes) Populations

“…Impaired DSB repair was previously elucidated in the cells derived from a radiation-sensitive strain of medaka using immunofluorescence staining of γ-H2AX and phosphorylated DNA-PK at T2609 [15]. Recently, there are several studies using medaka to analyze the functional differences among genetic polymorphisms for understanding those in humans [16–18]. Since medaka has highly differentiated geographical populations with large genetic diversity [19], the similar genetic polymorphisms equivalent to humans are occasionally found in the wild populations of medaka.…”