Our Stolen Futurea book by Theo Colborn, Dianne Dumanoski, and John Peterson Myers


  Nagler JJ, J Bouma, GH Thorgaard, and DD Dauble. 2001. High Incidence of a Male-Specific Genetic Marker in Phenotypic Female Chinook Salmon from the Columbia River. Environmental Health Perspectives 109:67-69.


Nagler et al. report an unexpectedly and unusually high proportion of wild chinook salmon that appear to have been sex-reversed early in development: chromosomal males that have female reproductive tracts. Genetically-similar hatchery-raised salmon in another river show no such effect. This research raises the question as to whether widespread sex-reversal may be contributing to the decline in wild salmon populations in the Pacific Northwest.

Feminization of male fish has been focal point of concern about endocrine disruption since the early 1990s. While the phenomenon was first discovered in England, it is now also known to occur widely in Europe and in the United States. This paper is the first to report feminization in an endangered salmon. It is also striking because of the high proportion of feminized males and the degree to which sex reversal has gone: many of the males are fully fertile females.

Experiments with other species of fish have shown that exposure of fish eggs to estrogen-mimicking substances can cause complete sex reversal of males to fertile females.

What did they do?
Nagler et al. sampled male and female spawning salmon in the Hanford Reach of the Columbia River in central Washington state to determine whether apparent males and females were in fact genotypically males and females. Sex in salmon is determined chromosomally: females are XX and males are XY. Nagler et al. tested for the presence of a genetic marker present only in XY individuals. Under normal circumstances, an individual with this genetic marker would grow up male.

They sampled from three separate spawning grounds in the Hanford Reach and also obtained samples from two reference populations, both hatchery fish runs in Idaho. One of these runs was established from the genetic stock of salmon spawning naturally at Hanford Reach.

What did they find?
84% of phenotypic females in the wild salmon tested positive for the male genetic marker. In contrast, none of the hatchery raised females tested positive.

Nagler et al. consider possible causes for this sex reversal and identify two strong candidates. One involves abnormally high water temperatures on the spawning grounds. Laboratory research with a closely related species of salmon has shown that increases in temperature can alter the sex ratio of the offspring, and water temperatures in the Hanford Reach are affected by water management protocols at dams upstream from these spawning grounds.

The second possibility is that contamination by endocrine disrupting compounds may have feminized the developing males. According to Nagler et al.:


An estrogen-sensitive "window" in salmonids occurs around the time of hatching and extends to beyond the time when these fish begin to feed exogenously; during this window male chinook salmon have been shown to be very susceptible to sex reversal. Early during this estrogen-sensitive period (at or shortly after hatching) male chinook salmon can be sex reversed by exposure to high concentrations of estrogen for periods as short as one hour. ...

It is possible that wild chinook salmon in the Hanford Reach were exposed to estrogens or compounds that mimic the biological activity of estrogens--the so-called environmental estrogens that have caused sex reversal in some genotypic males. Environmental estrogens are chemicals in the form of detergents, plasticizers, and pesticides that derive from a wide range of human activities, such as industry, agriculture, and domestic sewage processing. Some of these compounds (e.g., atrazine, carbofuran, lindane, methyl parathion, and dieldrin), known to be estrogenic in rainbow trout (O. mykiss) bioassays, are present in the Columbia River. The compounds identified have been detected throughout the year in waters of the Hanford Reach at annually stable but low levels (> 1-6 ng/L)


Nagler et al. go on to speculate that it is possible that the small percentage of "real" females in the wild chinook sample were from an upstream hatchery. They also note that the offspring spawned by mating of real males with sex-reversed males would be either XY or YY instead of all XY, the outcome of normal male to normal female mating. YY would never happen normally. This would lead to a steady decrease in the number of normal females in the population. The fact that only 16% of females were normal (and some if not all of those may have been hatchery, not wild), appears consistent with that prediction.





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