Impact of light pollution at night on male reproductive success in Japanese medaka (Oryzias latipes)

Abstract

Environmental light is perceived and anticipated by organisms to synchronize their biological cycles. Therefore, exposure to artificial light at night could disrupt diurnal and seasonal rhythmicity. Reproduction is a complex physiological process involving integration of environmental signals by the brain, and release of endocrine signals by the pituitary that regulate gametogenesis and spawning. In addition, males from many species form a dominance hierarchy that, through a combination of aggressive and protective behavior, influences their reproductive success. In this study, we investigated the effect of different light regimes, including light pollution at night and continuous light, on the fitness of male fish within a dominance hierarchy using a model fish, the Japanese medaka. In normal light/dark rhythm conditions, we observed that dominant males are more aggressive, remain closer to the female, and spend ten-fold more time spawning than subordinates. By using males with different genotypes, we determined the paternity of the progeny and found that even though subordinate males spend less time with the females, they are equally successful at fertilizing eggs in normal light conditions due to an efficient sneaking behavior. However, when exposed to light at night, dominant males fertilize more eggs. We indeed found that when exposed to nocturnal light pollution, dominant males produce higher quality sperm than subordinate males. Surprisingly, we did not find differences in circulating sex steroid levels, pituitary gonadotropin levels, or gonadosomatic index between dominant and subordinate males, neither in control nor night light condition. Continuous light was found to completely inhibit establishment of male hierarchy. This study is the first to report an effect of light pollution on sperm quality with an impact on male fertilization success in any vertebrate. It has broad implications for fish ecology in urban areas with potential impacts on the genetic diversity of these fish populations. GRAPHICAL ABSTRACT O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=95 SRC="FIGDIR/small/536935v1_ufig1.gif" ALT="Figure 1"> View larger version (27K): org.highwire.dtl.DTLVardef@149072dorg.highwire.dtl.DTLVardef@1763cd7org.highwire.dtl.DTLVardef@194586aorg.highwire.dtl.DTLVardef@38c518_HPS_FORMAT_FIGEXP M_FIG C_FIG HighlightsO_LIIn a triadic relationship, subordinate medaka show sneaking behavior during female spawning, allowing them to produce about 50% of the offspring. C_LIO_LIContinuous light inhibits establishment of male hierarchy. C_LIO_LILight pollution at night shifts the balance of reproductive efficiency between dominant and subordinate males, benefiting dominant males. C_LIO_LIExposure to light pollution at night improves sperm quality in dominant fish relative to subordinates, but does not clearly affect reproductive hormone levels. C_LI