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Abstract Convergent evolution is pervasive in nature, but it is poorly understood how various constraints and natural selection limit the diversity of evolvable phenotypes. Here, we analyze the transcriptome across fruiting body development to understand the independent evolution of complex multicellularity in the two largest clades of fungi—the Agarico- and Pezizomycotina. Despite >650 My of divergence between these clades, we find that very similar sets of genes have convergently been co-opted for complex multicellularity, followed by expansions of their gene families by duplications. Over 82% of shared multicellularity-related gene families were expanding in both clades, indicating a high prevalence of convergence also at the gene family level. This convergence is coupled with a rich inferred repertoire of multicellularity-related genes in the most recent common ancestor of the Agarico- and Pezizomycotina, consistent with the hypothesis that the coding capacity of ancestral fungal genomes might have promoted the repeated evolution of complex multicellularity. We interpret this repertoire as an indication of evolutionary predisposition of fungal ancestors for evolving complex multicellular fruiting bodies. Our work suggests that evolutionary convergence may happen not only when organisms are closely related or are under similar selection pressures, but also when ancestral genomic repertoires render certain evolutionary trajectories more likely than others, even across large phylogenetic distances.
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Divergence time and environmental similarity predict the strength of morphological convergence in stick and leaf insects
Independent evolution of similar traits in lineages inhabiting similar environments (convergent or repeated evolution) is often taken as evidence for adaptation by natural selection, and used to illustrate the predictability of evolution. Yet convergence is rarely perfect for two reasons. First, environments may not be as similar as they appear. Second, responses to selection are contingent upon available genetic variation and independent lineages may differ in the alleles, genetic backgrounds, and even the developmental mechanisms responsible for the phenotypes in question. Both impediments to convergence are predicted to increase as the length of time separating two lineages increases, making it difficult to discern their relative importance. We quantified environmental similarity and the extent of convergence to show how habitat and divergence time each contribute to observed patterns of morphological evolution in 212 species of stick and leaf insects (order Phasmatodea). Dozens of phasmid lineages independently colonized similar habitats, repeatedly evolving in parallel directions on a 23-trait morphospace, though the magnitude and direction of these shifts varied. Lineages converging toward more similar environments ended up closer on the morphospace, as did closely related lineages, and closely related lineages followed more parallel evolutionary trajectories to arrive there than more distantly related ones. Remarkably, after accounting for habitat similarity, we show that divergence time reduced the extent of convergence at a constant rate across more than 100 My of separation, suggesting even the magnitude of contingency can be predictable, given sufficient spans of time.
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- Award ID(s):
- 2015907
- PAR ID:
- 10589901
- Publisher / Repository:
- US National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 122
- Issue:
- 1
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2319485121
