Genomic evidence for sexual traits as honest indicators of immune function in birds?

Recent study reports correlated evolution of immune and pigmentation genes.

Charles Darwin famously wrote: “The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!” He was referring to the fact that the elaborate tail of this colorful bird could not be explained by his recently published theory of natural selection. How could such a clumsy feature improve the survival chances of a male peacock? Later on, Darwin proposed a solution to this conundrum in another book The Descent of Man, and Selection in Relation to Sex: sexual selection. According to this mechanism, males compete for access to females, either directly through male-male competition (think of the antlers of male deer) or indirectly by advertising themselves with beautiful songs and extravagant feathers.

But how do females make a choice? Some authors have argued that females pick a partner based on aesthetic preferences; females just select what they “like”. Richard Prum has defended this neutral model of sexual selection in his book The Evolution of Beauty. Alternatively, the elaborate traits of males are honest signals that females use to discriminate between males with “good” and “bad” genes. One particular hypothesis – proposed by William Hamilton and Marlene Zuk – suggests that sexual traits indicate the immune function of a bird. Males that can easily fend off parasites will have plenty of energy left to develop extravagant feathers, while males infected with parasites will look drab and sickly. A recent study in the journal Frontiers in Ecology and Evolution tested this Hamilton-Zuk hypothesis with genomic data.

Purifying Selection

Shubham Jaiswal and his colleagues used a set of eleven high-quality bird genomes to gain more insights into the genomic basis of sexual selection. First, they estimated the strength of sexual selection for each species, making a distinction between pre-copulatory selection (i.e. females picking a partner) and post-copulatory selection (i.e. sperm competition). Pre-copulatory selection was estimated by scoring the degree of sexual dimorphism: the more different males and females look, the stronger sexual selection. For example, the Indian Peafowl (Pavo cristatus) scored high for this index, while the Budgerigar (Melopsittacus undulatus) had the lowest score. Post-copulatory selection could be assessed through the ratio of testis to body weight. Species with fierce sperm competition need to produce more sperm cells and will probably have bigger testes.

These two measures of sexual selection – sexual dimorphism and testis weight – were consequently correlated with several parameters of gene evolution, such as substitution rates and estimates of selection. The analyses resulted in a set of 60 candidate genes that are potentially targets of sexual selection. Interestingly, most of these genes are involved in the regulation of gene expression and some are known to coordinate the development of sexual dimorphism. Additional tests of selection indicated that the majority of these genes are subject to purifying selection, the removal of (slightly) deleterious genetic variants. This evolutionary model is in line with the Hamilton-Zuk hypothesis where males with inferior immune systems are selected against.

An overview of the genomic resources used in this study (Figure A) and an example of variation in sexual dichromatism scores (Figure B). From: Jaiswal et al. (2021) Frontiers in Ecology and Evolution.

Correlated Evolution

The observation of purifying selection on the candidate genes might make sense within the framework of the Hamilton-Zuk hypothesis. However, it is not direct evidence for this controversial idea. The most convincing piece of evidence came from a second set of analyses, namely patterns of correlated evolution between different genes. The researchers identified 228 genes that showed significant signs of correlated evolution and had well-defined functional annotations. Within this network of correlated evolution, many gene pairs were involved in immunity and feather development or pigmentation. Based on these findings, the researchers noted that:

[This] provides a “mechanistic link” or a connection between genome and phenotypic coevolution which in such cases would include plumage color and other secondary sexual characters responsible for sexual selection and honest signaling. Therefore, the Hamilton-Zuk explanation for the persistence of variation in the phenotypes of sexual selection as a consequence of the arms-race between parasite and immune genes is substantiated by this study.

However, it is important to keep in mind that these are correlations. Remember the age-old warning: correlation is not causation. These candidate genes are a promising starting point for future research, but we should not jump to conclusions. There is still much to learn about the genetic basis of sexual selection, whether it involves the immune system or not.

A network representation of gene pairs showing patterns of correlated evolution (Figure A). And a section of this network where only the immune-related, feather-related, and pigmentation-related are shown (Figure B). From: Jaiswal et al. (2021).

References

Jaiswal, S. K., Gupta, A., Shafer, A., PK, V. P., Vijay, N., & Sharma, V. K. (2021). Genomic Insights Into the Molecular Basis of Sexual Selection in Birds. Frontiers in Ecology and Evolution, 2.

Featured image: Indian Peafowl (Pavo cristatus) © Gabriel Castaldini | Wikimedia Commons

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