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Synopsis The proliferation of genomic resources for Chelicerata in the past 10 years has revealed that the evolution of chelicerate genomes is more dynamic than previously thought, with multiple waves of ancient whole genome duplications affecting separate lineages. Such duplication events are fascinating from the perspective of evolutionary history because the burst of new gene copies associated with genome duplications facilitates the acquisition of new gene functions (neofunctionalization), which may in turn lead to morphological novelties and spur net diversification. While neofunctionalization has been invoked in several contexts with respect to the success and diversity of spiders, the overall impact of whole genome duplications on chelicerate evolution and development remains imperfectly understood. The purpose of this review is to examine critically the role of whole genome duplication on the diversification of the extant arachnid orders, as well as assess functional datasets for evidence of subfunctionalization or neofunctionalization in chelicerates. This examination focuses on functional data from two focal model taxa: the spider Parasteatoda tepidariorum, which exhibits evidence for an ancient duplication, and the harvestman Phalangium opilio, which exhibits an unduplicated genome. I show that there is no evidence that taxa with genome duplications are more successful than taxa with unduplicated genomes. I contend that evidence for sub- or neofunctionalization of duplicated developmental patterning genes in spiders is indirect or fragmentary at present, despite the appeal of this postulate for explaining the success of groups like spiders. Available expression data suggest that the condition of duplicated Hox modules may have played a role in promoting body plan disparity in the posterior tagma of some orders, such as spiders and scorpions, but functional data substantiating this postulate are critically missing. Spatiotemporal dynamics of duplicated transcription factors in spiders may represent cases of developmental system drift, rather than neofunctionalization. Developmental system drift may represent an important, but overlooked, null hypothesis for studies of paralogs in chelicerate developmental biology. To distinguish between subfunctionalization, neofunctionalization, and developmental system drift, concomitant establishment of comparative functional datasets from taxa exhibiting the genome duplication, as well as those that lack the paralogy, is sorely needed.
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Multimerization variants as potential drivers of neofunctionalization
Whole-genome duplications are common during evolution, creating genetic redundancy that can enable cellular innovations. Novel protein-protein interactions provide a route to diversified gene functions, but, at present, there is limited proteome-scale knowledge on the extent to which variability in protein complex formation drives neofunctionalization. Here, we used protein correlation profiling to test for variability in apparent mass among thousands of orthologous proteins isolated from diverse species and cell types. Variants in protein complex size were unexpectedly common, in some cases appearing after relatively recent whole-genome duplications or an allopolyploidy event. In other instances, variants such as those in the carbonic anhydrase orthologous group reflected the neofunctionalization of ancient paralogs that have been preserved in extant species. Our results demonstrate that homo- and heteromer formation have the potential to drive neofunctionalization in diverse classes of enzymes, signaling, and structural proteins.
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- Award ID(s):
- 1951819
- PAR ID:
- 10230885
- Date Published:
- Journal Name:
- Science Advances
- Volume:
- 7
- Issue:
- 13
- ISSN:
- 2375-2548
- Page Range / eLocation ID:
- eabf0984
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1126/sciadv.abf0984
