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