Abstract
Perchlorate is a common aquatic contaminant that has long been known to affect thyroid function in vertebrates, including humans. More recently perchlorate has been shown to affect primordial sexual differentiation in the aquatic model fishes zebrafish and threespine stickleback, but the mechanism has been unclear. Stickleback exposed to perchlorate from fertilization have increased androgen levels in the embryo and disrupted reproductive morphologies as adults, suggesting that perchlorate could disrupt the earliest stages of primordial sexual differentiation when primordial germ cells (PGCs) begin to form the gonad. Female stickleback have three to four times the number of PGCs as males during the first weeks of development. We hypothesized that perchlorate exposure affects primordial sexual differentiation by reducing the number of germ cells in the gonad during an important window of stickleback sex determination at 14–18 days post fertilization (dpf). We tested this hypothesis by quantifying the number of PGCs at 16 dpf in control and 100 mg/L perchlorate-treated male and female stickleback. Perchlorate exposure from the time of fertilization resulted in significantly reduced PGC number only in genotypic females, suggesting that the masculinizing effects of perchlorate observed in adult stickleback may result from early changes to the number of PGCs at a time critical for sex determination. To our knowledge, this is the first evidence of a connection between an endocrine disruptor and reduction in PGC number prior to the first meiosis during sex determination. These findings suggest that a mode of action of perchlorate on adult reproductive phenotypes in vertebrates, including humans, such as altered fecundity and sex reversal or intersex gonads, may stem from early changes to germ cell development.
Highlights
Perchlorate is a common aquatic contaminant that has been shown to affect thyroid function by competitively inhibiting iodide uptake at the sodium-iodide symporter [1]
We examine whether the earliest known morphological marker of sex determination in stickleback, primordial germ cell (PGC) number, is affected by perchlorate exposure beginning at fertilization
We found that perchlorate exposure decreases primordial germ cell number in female stickleback at 16 dpf, a time when genetic signaling cascades involving germ cell number are important to sex determination
Summary
Perchlorate is a common aquatic contaminant that has been shown to affect thyroid function by competitively inhibiting iodide uptake at the sodium-iodide symporter [1]. This small molecule has been linked to a variety of developmental abnormalities associated with hypothyroidism in humans, including reduced cognitive function [2, 3]. In addition to its effects on thyroid development and function, perchlorate appears to act through an unknown mechanism to alter gonad development and sex determination in teleost fishes, a finding not predicted to occur solely via thyroid disruption [4, 6, 8, 11, 15]. In contrast to our findings in stickleback, exposure of zebrafish to perchlorate during early development skews the sex ratio towards female [15], suggesting some species-specific effects of perchlorate on sexual development
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