Search bioRxiv⌕ Search

bioRxiv · 10.1101/2022.03.10.483751

Dynamic evolution of recently duplicated genes in Caenorhabditis elegans

Abstract

As a major origin of evolutionary novelties, gene duplication is a widespread phenomenon across species. However, the evolutionary force that determines the fate of duplicate genes is still under debate. Here, we studied the functional evolution of duplicate genes at both macroevolution and microevolution scales using the genomic sequences of eleven Caenorhabditis species and 773 C. elegans wild isolates. We found that compared to older duplicate genes and single-copy genes, recently duplicated gene copies showed rapid turnover, large genetic diversity, and signs of balancing and positive selection within the species. Young duplicate genes have low basal expression restricted to a few tissues but show highly responsive expression towards pathogenic infections. Recently duplicated genes are enriched in chemosensory perception, protein degradation, and innate immunity, implicating their functions in enhancing adaptability to external perturbations. Importantly, we found that young duplicate genes are rarely essential, while old duplicate genes have the same level of essentiality as singletons, suggesting that essentiality develops over a long time. Together, our work in C. elegans demonstrates that natural selection shapes the dynamic evolutionary trajectory of duplicate genes. SignificanceThe "evolution by gene duplication" theory suggests that gene duplications provide the genetic materials for mutation and selection to act upon, expand the repertoire of molecular functions, and enable evolutionary novelty. Although various models were proposed to describe the fate of duplicate genes, empirical evidence for these models is limited. We analyzed gene duplications in eleven nematode Caenorhabditis species and studied the intraspecific variation of these duplicate genes among C. elegans wild strains. We found that compared to older duplicate gens and single-copy genes, recently duplicated genes show rapid turnover, large genetic diversity, and strong signs of balancing and positive selection but rarely develop essential functions. Our results describe the evolutionary trajectory of duplicate genes shaped by natural selection.

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Ma, F., Lau, C. Y., Zheng, C.. 2022-03-12. Dynamic evolution of recently duplicated genes in Caenorhabditis elegans. https://doi.org/10.1101/2022.03.10.483751

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

A Deep Phylogenetic Split Between Short- and Long-Wavelength-Tuned Visual Systems in Surgeonfishes (Acanthuridae)

The light environment, coupled with ecology, is widely thought to drive visual adaptation, creating species-specific visual niches. However, coral reef ecosystems experience continuous spatiotemporal variations in light conditions, and mechanisms such as phenotypic plasticity may be essential for coral reef animals to adjust to such changing sensory requirements. It remains unclear how widespread colour vision plasticity is, or the extent to which ecology and phylogeny drive plasticity in coral reef fishes. Using a comparative transcriptomic approach across 22 species, we aimed to investigate visual plasticity within a prominent coral reef fish family, surgeonfishes (Acanthuridae), in response to changes in the light environment throughout development and across seasons in adults. Surprisingly, we uncovered a deep phylogenetic split (~42 mya) in visual opsin gene expression profiles, with Nasinae expressing a shorter-shifted palette than Acanthurinae, which coincides with the divide between water-column and benthic-feeding modalities during the speciation of their last common ancestor. However, opsin gene expression showed little variation in response to seasonal or ontogenetic shifts in the light environment, nor in the broad functional feeding groups extant species from both subfamilies fall under. Thus, the invariable visual gene expression observed in present-day surgeonfishes appears to be dictated by phylogenetic inertia, despite rapid diversification into a range of ecological niches. This suggests that spectral tuning into two main modalities, short and long, reduces the need for visual plasticity, allowing larger and more mobile coral reef fishes to conduct visually guided behaviours across the entire range of light environments they encounter.

evolutionary biology↗

Efficient growth factor production stabilizes cooperation in a cellular public goods game

Eukaryotic cells secrete growth factors that facilitate the proliferation and survival of neighboring cells in a coordinated manner essential for tissue development, repair, and homeostasis. However, mutant cells that fail to produce these factors may exploit the benefits provided by neighboring producers, thereby gaining a proliferative advantage that could lead to the extinction of the producer clone. Evolutionary theory predicts that preventing this "tragedy of the commons" requires a fixed spatial structure or other mechanisms that enable cells to interact preferentially with copies of themselves. Contrary to this expectation, we found that, in competition experiments, cells producing the diffusible growth factor interleukin-3 (IL3) resist invasion by non-producing mutant cells even in well-mixed populations, and that non-producers are driven to extinction instead. Using evolutionary game theory, we show that this outcome arises when the cost-to-benefit ratio of growth factor production falls below a critical threshold. We derive this tipping point analytically across the full parameter space of benefit function shape and group size and confirm that IL3 production in our experimental system satisfies this condition with a production cost less than 0.1% of the benefit conferred. These results demonstrate that efficient public good production alone can resolve the tragedy of the commons in populations of cells, and potentially in other biological systems.

evolutionary biology↗

Repeated Transitions in Migratory Behavior Across a Songbird Radiation Are Not Driven by Selection on Shared Variation in Candidate Genes

Understanding the mechanisms facilitating the repeated evolution of traits is a core question in evolutionary biology. While repeated evolution has been observed across many systems, behavioral phenotypes have been less well studied than morphological traits. Migration is a behavioral adaptation to seasonality that has evolved independently in many animals, and repeated gains and losses of migratory behavior have been especially prevalent throughout the diversification of birds. While migratory traits are heritable in many taxa and candidate genes underlying intraspecific variation in migratory behavior have been identified, whether similar genetic changes are responsible for the repeated evolution of migration remains poorly understood. We used a phylogenomic approach to investigate the relationship between variation in candidate genes and migratory propensity across nearly all species in the parulid warbler radiation (n = 101), a group of songbirds in which migratory behavior has been lost and gained multiple times. Comparisons of candidate gene tree topologies to the parulid warbler species tree revealed cases of discordance, though these were explained by differences in the number of phylogenetically informative sites among genes rather than by elevated genetic similarity among species sharing migratory strategies. Testing models of coding sequence evolution identified sites with elevated dN/dS in five candidate genes, suggestive of positive selection; however, variation at these sites showed no clear association with migratory strategy, nor did we detect recurrent selection across lineages where transitions in migratory behavior most likely occurred. Together, these results contradict the hypothesis that selection on shared variation (ancestral polymorphisms or introgressed alleles) facilitated the repeated evolution of migration in this clade.

evolutionary biology↗