The significance of sex ratio biasing to evolutionary biology
Jonty Haywood
August 2008
Introduction
This paper makes three key proposals:
1. Sex ratio biasing explicitly undermines neo-Darwinian theory.
2. Genotype biasing will not be limited to offspring sex determination.
3. Genotype biasing will involve environmentally-modified genotype-linked segregation distorters.
There is now significant evidence from a variety of mammalian species that parents can bias the sex ratio of their offspring depending on environmental factors (Trivers-Willard theory and the local-resource competition model). The premise of this paper is that sex ratio biasing explicitly undermines neo-Darwinian theory, and that there is no reason to assume that such genotype biasing is limited to offspring sex determination. Parents will use equivalent mechanisms to bias any offspring genotypes depending on their environment. Just as a well-fed hamster or high-ranking deer is more likely to have male offspring, a parent living in a darker than usual environment will be more likely to have offspring with darker than expected fur, a parent living in a colder environment will be more likely to have offspring with thicker fur and so on. Such adaptations will occur not only over many generations through natural selection, but in the very next generation.
Genotype biasing must involve segregation distorter genes, and this paper proposes a mechanism involving segregation distorters which are both indirectly modified by the parent environment and linked to genes for appropriate phenotypes. Such a mechanism could be used to benefit the entire genome, not just those genes linked to the segregation distorter, and as such would be widespread in sexually-reproducing organisms.
Any comments, suggestions or criticisms would be greatly appreciated. Please contact me at mail@losethegame.com
Evidence of offspring genotype ratio biasing by parent environment
Trivers-Willard theory:
Theory and data suggest that a male in good condition at the end of the period of parental investment is expected to outreproduce a sister in similar condition, while she is expected to outreproduce him if both are in poor condition. Accordingly, natural selection should favor parental ability to adjust the sex ratio of offspring produced according to parental ability to invest. Data from mammals support the model: As maternal condition declines, the adult female tends to produce a lower ratio of males to females. (Trivers, R.L., & Willard, D.E. (1973). Natural selection of parental ability to vary the sex ratio of offspring. Science, 179, 90-92. )
This has been documented in Venezuelan opossums (Austad and Sunquist 1986) and hamsters (Clutton-Brock and Iason 1986; Clutton-Brock 1991; Huck, Labov and Lisk 1986).
A similar phenomenon, known as the local-resource competition model, has shown sex ratio bias determined by the social rank of the parent and the rank inheritance pattern for the species. High-ranking females of species in which rank is inherited by male offspring (female exogamous species), such as red deer (Clutton-Brock, Albon and Guinness 1984) and spider-monkeys (Symington 1987), are more likely to have male offspring. High-ranking females of species in which rank is inherited by female offspring (male exogamous species), such as baboons (Altmann 1980), macaques (Silk 1983; Simpson and Simpson 1982; Small and Hrdy 1986) and howler monkeys (K. Glander), are more likely to have female offspring.
Segregation distortion
Segregation distorter genes increase their own chances of being passed into offspring, biasing offspring genotype ratio in their favour. They are classed as outlaws as they are assumed to be deleterious to genome fitness for at least two reasons:
They distort gametogenesis by inhibiting gamete efficacy.
They reduce randomisation of alleles, reducing immunity to parasites.
A segregation distorter will benefit other genes in proportion to their linkage to the segregation distorter itself. Pressure for outlaw-suppressing genes, known as modifiers, that suppress the deleterious effects of segregation distorters, will exist in relatively non-linked regions of the genome. At any given locus, the pressure for a modifier gene to evolve will increase with the cost of segregation distortion to that gene, and decrease with linkage between the gene and the segregation distorter. Therefore, a segregation distorter will be surrounded be a region of decreasingly linked genes which benefit from the distortion, and where modifiers are selected against, which, in turn, is surrounded by genes which are exploited by distortion, and where modifiers are selected for. Segregation distortion will be especially costly when linked to genes involved in parasite immunity such as the major histocompatability complexes or other surface proteins.
Biasing offspring genotype with environmentally-modified genotype-linked segregation distorters
The mechanism by which sex ratios are biased must involve sex-linked segregation distorters which are activated by environmental factors such as parent condition or social rank. (It should be noted that activation of a segregation distorter is equivalent to the suppression of its modifiers)
Parent condition/rank ---> Activates sex-linked segregation distorter ---> Biased sex ratio
In other words, offspring genotype is being adjusted depending on the enviroment of the parent. However, there is no reason to assume that environmentally-adjusted segregation distorters will solely be sex-linked, they could be linked to any allele for any phenotypic effect. As such, every phenotypic effect may be adjusted according to the parent environment.
Parent environment ---> Activates genotype-linked segregation distorter ---> Biased ratio of phenotypes
Modifying segregation distortion according to stimuli from the parent environment can reduce the cost of a segregation distorter to genome fitness. This parent-environment -> offspring-genotype control system would benefit genome fitness by selecting gametes that are likely to become higher fitness offspring according to the parent environment. It should be noted that although such benefits could outweigh the deleterious effects of the segregation distortion entirely so that modifiers could exist in regions of the genome not linked to the segregation distorter, such modifiers would be more likely to evolve in regions of the genome linked to the segregation distorter.
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Conclusion
Rather than segregation distortion being limited to a few outlaw genes under constant suppression from the rest of the genome, the genome suppresses them selectively depending on which alleles they are linked to and on the parent environment. This provides a mechanism whereby offspring genotype, and hence phenotype, can be adjusted according to parent environment. The genomes of sexually-reproducing organisms will contain complex networks of such segregation distorters and environmentally-responsive modifiers. This mechanism could be involved in adjusting every aspect of the genotypes of every sexually-reproducing organism.
Regardless of whether this mechanism is actually involved, the fundamental message of this paper is that sex ratio biasing explicitly undermines neo-Darwinian theory, and that there is no reason to assume that such genotype biasing is limited to offspring sex determination.
Hypothetical examples
Example 1. Parent visual environment -----> Offspring coat colour
A hormone (such as melatonin) signals long-term light intensity based on parent visual sensation. A segregation distorter is linked to an allele for dark coat pigment. A modifier mutates so that its suppression of the segregation distorter is proportional to the hormone concentration.
In a dark environment, the segregation distorter is not suppressed, biasing offspring with dark coats.
An interesting variation of this could involve an animal whose predators see a shifted spectrum, in UV, for example. This would make it beneficial for the organism to sense UV for segregation distorter modification, even though the organism doesn't ever perceive UV consciously itself.
Example 2. Parent MHC environment -----> Offspring MHC
Pheromones signal which MHC alleles other individuals possess. An MHC allele is linked to a segregation distorter. The segregation distorter is suppressed if levels of pheromones for that MHC are high.
This system would increase the frequency of rare MHC alleles in the next generation, providing improved immunity to parasites.
It should be noted that a MHC-linked segregation distorter would usually be highly deleterious to the genome. However, with the involvement of an environmentally responsive modifier, this system could be more effective at improving immunity than the currently-accepted randomising Mendelian method.
Example 3. Parent condition -----> Offspring growth pattern (non-sex-linked Trivers & Willis theory)
Example 4. Parent social rank -----> Offspring social behaviour (non-sex-linked local-resource competition model)
Simulation Testing
I am working on an evolution simulator to investigate the possible benefits of this mechanism. The current version only simulates asexual organisms, I have yet to include sexual reproduction and segregation distorter genes. It can be found at http://losethegame.com/evosim/