Whether one is genetically born as male or female is decided when the sperm meets the egg. It is only under unique conditions that Mother Nature would divert from such a rule in mammals. This is not the case in fish, where the environment can influence the sex that an animal assumes later in life. Working with sea lamprey (Petromyzon marinus), Nicholas Johnson from the US Geological Survey at Hammond Bay Biological Station in Michigan and colleagues from the Department of Fisheries and Wildlife at Michigan State University serendipitously identified additional factors that influence whether a fish becomes male or female in the wild.

Sea lampreys – which have retained most of their ancestral characteristics from over 500 million years ago – undergo a complex life cycle. Most of a lamprey's life is spent as an earthworm-like larva in rivers and streams, where it resides in sediments, feeding on algae and decomposing material for 3–7 years. Once it reaches a certain size, it stops feeding and goes through a restructuring of its body, in a process called metamorphosis, before migrating to the Great Lakes or the ocean, where it feeds on large fishes and matures. Once maturation is complete, it then migrates to upstream rivers to spawn. Whether a lamprey becomes male or female is determined before it undergoes metamorphosis, but little is known about what influences sex assignment in this ancient fish.

While examining sea lamprey populations in the Great Lakes as part of a larger study to investigate rates of lamprey metamorphosis and survival in the Great Lakes tributaries, Johnson and colleagues collected larvae from the streams, tagged them and released them either directly into Great Lakes tributaries (nutrient-rich stream environment) or at the river mouth (nutrient-poor sluggish water environment). In the following years, the authors recaptured some of the larvae that had grown in those habitats, as well as the ones that had metamorphosed, matured and returned to spawn in the rivers. Johnson's team then compared the sex ratios of sea lampreys between the stream and slowly moving environments and found that in the nutrient-rich stream, the ratio of males to females was much lower than in the in nutrient-poor slow-moving water areas. In addition, the authors found that for sea lamprey that had metamorphosed 3 years after stocking, 56% of the population was male in the stream habitat and 78% was male in the poor-quality estuary habitat, suggesting that the level of nutrition in that habitat may influence sex assignment in this fish.

Using a probability model, Johnson and colleagues then calculated how likely it was that the animals reared in the nutrient-poor environment would become males and found that over 6 years, more than 90% of these lampreys would be male. To add to this observation, the authors reported that the animals reared in the nutrient-rich stream environment grew 2–4 times faster than those in the sluggish areas, making this the first study to link growth rate to sex determination in fish.

The effects of the environment, particularly those of temperature and social context (such as density) on sex ratios in fish have been well established, but it appears now that there are other players: nutrient level in the water and growth rate. It seems to me that when it comes to sex assignment in fishes, the Shakespearean phrase ‘To be or not to be’ gains a whole new meaning when you add the environment into the mix.

Johnson
,
S. J.
,
Swink
,
W. D.
and
Brenden
,
T. O.
(
2017
).
Field study suggests that sex determination in sea lamprey is directly influenced by larval growth rate
.
Proc. Biol. Sci.
284
,
20170262
.