The genetics of environmental sex determination

Sex is determined by your chromosomes, except when it isn't.

There is a well-established paradigm that the sex of some organisms is determined environmentally. This phenomenon is present in a range of plants and animals including some species in the angiosperms, mosses, ferns, fish, birds, reptiles, and nematodes.

This proposal will set out a logical argument, and a simple test, that will unequivocally challenge this paradigm in a nematode - with potentially far reaching consequences across the tree of life.

Plant-parasitic nematodes in several genera (namely here the Heterodera spp.) are born juvenile (sex-less). They enter a root of a host plant and establish a permanent feeding site within host tissue. To achieve this they deliver literally hundreds of "effectors" - proteins primarily - into the host. These effectors are exquisitely adapted to manipulate various aspects of host physiology, development, morphology, and immunity to establish the permanent feeding site. Once they start feeding, their sex is terminally assigned. They either develop into males, or they develop into females. It is commonly cited that sex of the nematode is determined by the interaction with the host: the ratio of males and females differs depending on the host genotype/status.

Consider the following two facts:

The nematode's genes (call them, a) determine the nematode's ability to exploit their host (call it, ß), such that ß depends on a.
Nematode sex (call it, ?) is depended on the nematode's ability to exploit their host (ß), such that ? depends on ß.
If ? depends on ß, and ß depends on a then, logically, ? depends on a: sex depends on genes. Therefore, maybe sex is determined by your genes, even when it apparently isn't.

Importantly, we can test this novel insight. We know that the genetic sequences of many effectors vary between individuals of a population. Some of these alleles will "function" on a given host, and some will not. It stands to reason then, that polymorphisms in genes which dictate the outcome of parasitism (e.g. effectors) will be "partitioned" into the sexes: for a given host genotype, individual juvenile nematodes with allele x will preferentially develop into males, while those with allele y will preferentially develop into females. Their sex was already determined by their genes.

To test this, we can individually sequence DNA from pools of juveniles pre-infection, and virgin males and females during infection. We would expect to identify genetic differences - i.e. poly-allelic sites with altered ratios in males or females compared to juveniles - that challenge the paradigm and elegantly highlight candidate genes that determined sex.

Simple, but undeniable, proof for the apparent contradiction in the title - a genetic basis of environmental sex determination.