Scientist from the Institute of Marine Science (ICM-CSIC), have just published an article that shows how in biology, form and function don’t always go hand in hand when it comes to fish gonads.
This article, published in Proceedings of the National Academy of Sciences of the United States of America (PNAS) with Laia Ribas as first author, is based on a study led by Francesc Piferrer in the ICM, in collaboration with scientists from the Temasek Life Sciences Laboratory, led by Laszlo Orbán in Singapore.
Scientist from the Institute of Marine Science (ICM-CSIC), have just published an article that shows how in biology, form and function don’t always go hand in hand when it comes to fish gonads.
This article, published in Proceedings of the National Academy of Sciences of the United States of America (PNAS) with Laia Ribas as first author, is based on a study led by Francesc Piferrer in the ICM, in collaboration with scientists from the Temasek Life Sciences Laboratory, led by Laszlo Orbán in Singapore.
Fish account for over half of living vertebrate species and are well known for having a very plastic sexual development and exhibit various forms of hermaphroditism.
Even in species with separate sexes, which are the majority, alterations of the environmental conditions during early development, for example, by being exposed to abnormally high temperatures, can result in a disproportionate number of males. This is because some genetic females end up differentiating as males. These masculinized females are called neomales and can skew sex ratios and threaten population survival in a global warming scenario.
Now, using several families of zebrafish, a species with separate sexes that is a popular research model for many areas of biology, researchers have found that the degree of masculinization as a response to elevated temperature is family-dependent.
Thus, some families are highly sensitive to heat, “indicating that the outcome is related to the interplay between genetics and environment. This is a nice example that reminds us that while organisms propose, the environment disposes”, explains Francesc Piferrer.
Females expresing ‘male’ gens
In the experiment, researchers exposed zebrafish larvae and juveniles to high-temperature ambients. As adults, heat-exposed fish were morphologically either males or females, as no intersex fish were observed based on the structure of the gonads. When scientists looked at the function —by analyzing the combined expression of all the genes in the gonads, the so-called ‘gonadal transcriptome’— among males they found males and neomales, as expected.
The surprise, however, came when they looked at the rest of the fish that despite being exposed to heat remained as females. There, scientists found actually two types of females: normal looking females, in terms of form and function, and females that despite having ovaries, were expressing mostly ‘male’ gens in their gonads.
Changes in function without changes in form
As Piferrer explains, “this means a major switch in gonad function in absence of change in organ form, a novel observation in vertebrates. Whether this occurs in natural populations of zebrafish or other species exposed to abnormally elevated temperatures is something that, at present, nobody knows”. But the discovery of highly heat-sensitive families and the presence of “undercover” males disguised as females, “means that we need to rethink our strategy of how we assess the effects of elevated temperatures on fish sex in a scenario of climate change”, he adds.
If females functioning as males were indeed found in natural populations, it would mean that we are currently underestimating the effects of global warming. Thus, in addition to looking at sex ratios (the form), “we would also need to look at the transcriptome (the function) to have a better estimate of the consequences”, Piferrer says. The immediate challenge is how to sample and identify these fishes while alive and to find out what happens at the time of reproduction.
Ribas, L., Liew, W.C., Díaz, N, Sreenivasan, R., Orban, L., Piferrer, F., 2017. Heat-induced masculinization in domesticated zebrafish is family-specific and yields a set of different gonadal transcriptomes. Proceedings of the National Academy of Sciences of the United States of America
NdP Delegación del CSIC de Cataluña