Feb. 28, 2012 Some animal and human populations were shown to shift their birth sex ratio from the expected unity. Using fluorescence in situ hybridisation, a research team lead by scientists from the Leibniz Institute for Zoo and Wildlife Research (IZW) now shows in a study that males in a captive endangered pygmy hippopotamus (Choeropsis liberiensis) population may be able to adjust the ratio of X- and Y-chromosome bearing spermatozoa in their ejaculates, in favour of producing more female offspring, as published in Nature Communications this week. The work reports that this could represent a way for the males to reduce competition for females from other males in this captive population.
There is evidence in some animal populations of the ability to shift the birth sex ratio from the expected equal ratio of male and female offspring. IZW scientist Dr Joseph Saragusty and colleagues studied a captive population of the endangered pygmy hippopotamus and found an excess of females, with only approximately 42% of the offspring born male. While most previous sex ratio shifts have been thought to be a consequence of female choice, the study shows for the first time that mammalian males shift the sex ratio of sperm in their ejaculates, in favour of X chromosomes. In this case, the authors suggest that it may be beneficial for the male to do this in order to reduce future competition for mating partners.
The issue of offspring sex determination has interested researchers for many centuries, yet, despite thousands of scientific studies conducted to date, the mechanism or mechanisms through which offspring sex ratios are shifted are still unknown. Studies have shown that under a wide variety of situations, animal and human populations may shift offspring, or secondary, sex ratio from the expected unity predicted by the random, equal opportunity both conceptus sexes have by nature. These shifts in secondary sex ratio have been attributed to factors such as maternal body condition, maternal diet quality and the level of sugar in circulation, maternal social status, population density, resource availability, mating rate, timing of copulation vis-à-vis ovulation, acute or chronic stress, timing along the mating season, or exposure to environmental contaminants such as polychlorinated biphenyl (PCB) or phytoestrogens.
Noting the difference between the sexes in terms of investment in offspring and the benefits gained thereby, it has been assumed that owing to its usually much larger investment, the female has considerably more to win or lose. Hence, if mechanisms to bias offspring sex ratios do exist, they would be operated by the female. In mammals, the female's oocytes all carry the X chromosome whereas the male's spermatozoa either carries an X or a Y chromosome and thus it is for the spermatozoon that fertilises the oocyte to determine the conceptus sex. Males produce their gametes through the process of spermatogenesis during which each progenitor cell that contains two sex chromosomes (an X and a Y) is divided to produce four spermatozoa -- two with X chromosome and two with Y. It was thus assumed that males deliver in their ejaculates approximately equal numbers of both sex chromosomes. Now, the research team lead by scientists from IZW showed that in the captive population of the pygmy hippopotamus, in which almost 58% of the offspring are females, males produce ejaculates that contain about the same proportion of spermatozoa carrying the X chromosome.
"While everybody was searching for the mechanism in the females, we decided to first determine whether the males have a say at all. By staining the X and Y chromosomes in the ejaculates with different fluorescence colours, we found that in all males investigated there were considerably more spermatozoa carrying the X chromosome," says Dr. Joseph Saragusty from the IZW who lead this study. This shift in ejaculate sex ratio, known as primary sex ratio, suggests that males do possess a mechanism to control the sex ratio of their ejaculates and thus participate in manipulating offspring sex.
The study is the first to suggest that mammalian males might possess a mechanism to modify population sex ratio. "Naturally, the male has no control over the fate of their ejaculates after mating so the final say is in the hands of the females," explains Dr. Saragusty, "however, by delivering considerably more spermatozoa of a certain sex, they can aim to increase the probability that one of these will fertilise the oocyte." Through an analysis of the different possible scenarios, the researchers conclude that in the study population of captive pygmy hippopotamus there appears little or no antagonistic sexual conflict, unexpected by prevailing theories.
„We still do not know through which mechanism the males adjust the sex ratio in their ejaculates, nor do we know what cues, environmental or other, cause them to activate this mechanism," adds Dr Robert Hermes of the IZW "but this could represent a way for the males to reduce male-male competition over mating opportunities." "If this mechanism is not unique to the pygmy hippopotamus but rather an integral part of male reproduction at large," adds Dr. Saragusty "it may provide an alternative explanation for a number of population sex ratio shifts, such as the excess in human male births, which hitherto have been ascribed to female cryptic choice alone."
This study was conducted in collaboration with a scientist from the Zoological Society of London in the UK and was supported by the German 2007 "Joint initiative for Research and Innovation" (Pakt) grant.
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- Joseph Saragusty, Robert Hermes, Heribert Hofer, Tim Bouts, Frank Göritz, Thomas B. Hildebrandt. Male pygmy hippopotamus influence offspring sex ratio. Nature Communications, 2012; 3: 697 DOI: 10.1038/ncomms1700
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