Jobling Susan, Coey S, Whitmore J G, Kime D E, Van Look K J W, McAllister B G, Beresford N, Henshaw A C, Brighty G, Tyler C R, Sumpter J P
Department of Biological Sciences, Brunel University, Kingston Lane, Uxbridge, Middlesex UB8 3PH, UK.
Biol Reprod. 2002 Aug;67(2):515-24. doi: 10.1095/biolreprod67.2.515.
Endocrine-disrupting chemicals, known to be present in the environment, have great potential for interfering with reproductive health in wildlife and humans. There is, however, little direct evidence that endocrine disruption has adversely affected fertility in any organism. In freshwater and estuarine fish species, for example, although a widespread incidence of intersex has been reported, it is not yet known if intersexuality influences reproductive success. The purpose of this study was, therefore, to determine gamete quality in wild intersex roach (Rutilus rutilus) by assessing sperm characteristics, fertilization success, and ability to produce viable offspring. The results clearly demonstrate that gamete production is reduced in intersex roach. A significantly lower proportion of moderately or severely feminized fish (17.4% and 33.3%, respectively) were able to release milt compared with normal male fish from contaminated rivers (in which 97.6% of the males were able to release milt), reference male fish (97.7%), or less severely feminized intersex fish (experiment 1: 85.8%, experiment 2: 97%). Intersex fish that did produce milt produced up to 50% less (in terms of volume per gram of testis weight) than did histologically normal male fish. Moreover, sperm motility (percentage of motile sperm and curvilinear velocity) and the ability of sperm to successfully fertilize eggs and produce viable offspring were all reduced in intersex fish compared with normal male fish. Male gamete quality (assessed using sperm motility, sperm density, and fertilization success) was negatively correlated with the degree of feminization in intersex fish (r = -0.603; P < 0.001) and was markedly reduced in severely feminized intersex fish by as much as 50% in terms of motility and 75% in terms of fertilization success when compared with either less severely feminized intersex fish or unaffected male fish. This is the first evidence documenting a relationship between the morphological effects (e.g., intersex) of endocrine disruption and the reproductive capabilities of any wild vertebrate. The results suggest that mixtures of endocrine-disrupting substances discharged into the aquatic environment could pose a threat to male reproductive health.
已知环境中存在的内分泌干扰化学物质极有可能干扰野生动物和人类的生殖健康。然而,几乎没有直接证据表明内分泌干扰对任何生物体的生育能力产生了不利影响。例如,在淡水和河口鱼类物种中,虽然已报告了广泛存在的雌雄同体现象,但尚不清楚雌雄同体是否会影响繁殖成功率。因此,本研究的目的是通过评估精子特征、受精成功率和产生可存活后代的能力,来确定野生雌雄同体拟鲤(Rutilus rutilus)的配子质量。结果清楚地表明,雌雄同体拟鲤的配子产量降低。与来自受污染河流的正常雄鱼(其中97.6%的雄鱼能够排出精液)、对照雄鱼(97.7%)或雌雄同体程度较轻的鱼(实验1:85.8%,实验2:97%)相比,中度或重度雌性化的鱼(分别为17.4%和33.3%)能够排出精液的比例显著更低。确实排出精液的雌雄同体鱼,其精液产量(以每克睾丸重量的体积计算)比组织学上正常的雄鱼少50%。此外,与正常雄鱼相比,雌雄同体鱼的精子活力(活动精子的百分比和曲线速度)以及精子成功使卵子受精并产生可存活后代的能力均有所降低。雄配子质量(通过精子活力、精子密度和受精成功率评估)与雌雄同体鱼的雌性化程度呈负相关(r = -0.603;P < 0.001),与雌雄同体程度较轻的鱼或未受影响的雄鱼相比,重度雌性化的雌雄同体鱼的雄配子质量在活力方面显著降低多达50%,在受精成功率方面降低多达75%。这是首个记录内分泌干扰的形态学效应(如雌雄同体)与任何野生脊椎动物生殖能力之间关系的证据。结果表明,排放到水生环境中的内分泌干扰物质混合物可能对雄性生殖健康构成威胁。