Is bigger better? Does whole genome duplication confer immune gene advantage in Corydoradinae catfishes.

Written by Ellen Bell, featured photo by Martin Taylor. Read the full paper here.

Whole genome duplication (WGD) or polyploidy is the process by which the entire nuclear genome of an organism is copied at least once. This can occur within species (autopolyploidy) or as a result of hybridisation between species (allopolyploidy). Polyploidisation events are relatively common in plants with an estimated 70% of flowering plants showing historical evidence of WGDs. However, this process is less common in the animal kingdom and its role in adaptation is still poorly understood.

The Corydoradinae are a group of neotropical catfishes which are widespread in freshwater rivers in tropical South America. They are a species-rich subfamily, with over 170 species divided into nine distinct evolutionary lineages. The Corydoradinae often coexist in mixed communities of up to three species, usually from different lineages. Previous studies have identified two WGD duplication events in the evolutionary history of the Corydoradinae (in addition to the fish specific WGD event that impacted all teleost fishes ~300 million years ago). The first Corydoras WGD event is estimated to have occurred 54-66 million years ago and affected lineages two to nine, and a more recent WGD estimated to have occurred 20-30 million years ago affected lineages six and nine. Following WGDs there are often large-scale genome rearrangements and rediploidisation – where the genome begins to return to a two-copy state via processes such as gene silencing, loss and fractionation (the loss of one gene copy). As a result, Corydoras species from lineage 1, which do not appear to have undergone a WGD (besides the teleost specific WGD) can be considered functionally diploid, whereas species in lineage 9 having undergone two WGDs more recently, will probably have begun the process of rediploidisation, but are still thought to be functionally polyploid. Corydoradinae live in mixed communities, often including species with different genome sizes and WGD histories coexisting within similar environmental conditions and pathogen exposures. This therefore makes them a unique system for examining adaptive differences relating to WGD.

Historically WGD has been perceived by some as an evolutionary dead-end and while this view is no longer generally subscribed to, the overall costs and benefits of WGD to fitness and ultimately to evolutionary success are still unclear. Our study was inspired by this knowledge gap and by a series of pioneering studies that suggested WGD could underpin evolutionary success. The specific direction of this study was then further informed by the unexpected observations obtained by an undergraduate student who noted that diploids had greater macro parasite loads than polyploids. A finding that sparked further questions about the immunogenetic backgrounds of the diploid and polyploid species. In theory, immune genes are excellent candidates to investigate fitness benefits of WGD. Several suites of immune genes have pathogen recognition receptors which are germ-line encoded and have broad specificities for binding to pathogens and which then initiate an immune response. Therefore, it may be expected that the additional immune gene copies generated by a WGD event could be beneficial, potentially expanding the pathogen recognition repertoire, or increasing the likelihood of heterozygote advantage or negative frequency dependence. For this study, we investigated variation at Toll-like receptors (TLRs), as they are part of the pathogen recognition receptor immune gene family and had previously been associated with parasitic infections in channel catfish.

Following this we investigated the differences in parasite load and immunogenetic diversity between a coexisting diploid and polyploid species of Corydoradinae (polyploid left and diploid right in the above photo). The first part of this project was validating initial observations from the preliminary study, finding that polyploid species had significantly fewer external parasites then diploid species from the same community. We next looked within our selected immune genes (a subset of the TLRs) for sequence variation and additional copy retention, and although we expected to find more variation in the polyploid species, the high level we observed was unforeseen. We also found that despite the probable pressures of rediploidisation, additional copies of the TLRs had been retained in most polyploid individuals.  Moreover, we also identified very low TLR variation in the diploid species which was comparable to populations of other vertebrates that had been through recent population bottlenecks. Overall, the evidence suggested that additional TLR copies were maintained in the polyploid species, suggesting exciting evidence for a potential adaptive advantage to be associated with WGD in a vertebrate system. Furthermore, these findings, although purely observational, highlight potential intriguing avenues of further enquiry regarding WGD, immune gene functionality, and pathogen exposures.

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