Genome Evolution: We are not so special
The most recent common ancestor of animals lived more than 600 million years ago, so we cannot sequence its genome. Nevertheless, we can identify a minimal set of gene families that were present in this long-dead ancestor by comparing genomic data across animals and their closest relatives. In addition to being interesting in its own right, this helps us identify which genes were gained and lost before the origin of animals and, likewise, which genes were gained and lost as animals diversified.
The challenge, though, is that there are strong sampling biases that can compromise these analyses. Genome sequencing has focused on species that are medically relevant, experimentally tractable, and easy to sequence (del Campo et al., 2014). Left unaddressed, these biases can frustrate efforts to reconstruct the genomes of our ancient ancestors. Take, for example, the simple case of three groups of organisms called O, C and M, and a gene that originated along the branch that gave rise to C and M (Figure 1A). If more sequencing effort has been invested in group M than in group C, the gene is more likely to be found in group M than in group C. And if the gene is found in M but not in C, even though it is present in both, then it will appear that the gene is specific to group M and younger than it actually is.
Now, in eLife, Daniel Richter, Parinaz Fozouni, Michael Eisen and Nicole King report their work to reduce sequencing bias by sampling many more genes in the sister group to animals, the choanoflagellates (Richter et al., 2018). They generated transcriptomic data for 19 species of choanoflagellates and analyzed them in combination with previously published metazoan (animal), choanoflagellate and other eukaryote genomes. In addition to presenting new data, Richter et al. – who are based at UC Berkeley, UCSF, the Gladstone Institutes and Station Biologique de Roscoff – applied new probabilistic methods to minimize the chance that a gene family would be predicted to be present in a taxonomic group based on the spurious assignment of unrelated genes to the same family.
In related work at the universities of Essex and Oxford, Jordi Paps and Peter Holland have reported an interesting analysis of gene gain and loss in early animal evolution (Paps and Holland, 2018). The studies agree on some key points. Both recovered a relatively large number of gene family gains along the ‘animal stem’ (the branch of the evolutionary tree that uniquely gives rise to animals; shown in blue in Figure 1B). However, while Paps and Holland estimate that the number of gains was much higher than the number of losses, which they interpreted as evidence for an accelerated expansion of gene families along the Metazoa stem, Richter et al. estimate approximately equal numbers of gains and losses (Figure 1C). This means that Richter et al. find evidence for accelerated churn of gene families along the Metazoa stem, not a burst of expansion. This incongruence is likely related to Paps and Holland analyzing two choanoflagellate species, compared to the 21 analyzed by Richter et al.
Another difference is that Paps and Holland did not estimate gene gain and loss along the Choanoflagellata stem, whereas Richter et al. did. This revealed more gene family gain and less gene family loss along the Choanoflagellata stem than along the Metazoa stem (Figure 1C). So, Richter et al. do find a burst of gene family expansion, but in Choanoflagellata rather than Metazoa. It will be critical to further test the findings of both studies with improved sampling of other closely related groups, which could change how the gains and losses are apportioned to these two stems.
The results presented by Richter et al. agree in important ways with other recent work (King et al., 2008; Suga et al., 2013). These analyses reveal that the genetic changes on the Metazoa stem included the evolution of new intercellular signaling pathways (Fairclough et al., 2013) and the integration of new ligands and receptors into intracellular pathways that were already present (such as the Hippo pathway; Sebé-Pedrós et al., 2012). Other changes included the expansion of a core set of transcription factors (de Mendoza et al., 2013), and increased cis-regulatory complexity (Sebé-Pedrós et al., 2016).
Comparative gene content analyses refine our understanding of what makes metazoans unique, and in the process we are learning about the underappreciated biology of our close non-metazoan relatives (Sebé-Pedrós et al., 2017). For instance, Richter et al. identified homologs of Toll-like receptors in most choanoflagellates. These genes were thought to be an animal-specific innovation for innate immunity. Future research could investigate if these genes have immune-like roles in non-animals.
It is impossible to know how special animals really are without also knowing something about our closest relatives. The more we learn about these relatives, the less special we seem to be.
References
-
The origin of animal multicellularity and cell differentiationDevelopmental Cell 43:124–140.https://doi.org/10.1016/j.devcel.2017.09.016
-
The others: our biased perspective of eukaryotic genomesTrends in Ecology & Evolution 29:252–259.https://doi.org/10.1016/j.tree.2014.03.006
-
The origin of Metazoa: a unicellular perspectiveNature Reviews Genetics 18:498–512.https://doi.org/10.1038/nrg.2017.21
-
The Capsaspora genome reveals a complex unicellular prehistory of animalsNature Communications 4:2325.https://doi.org/10.1038/ncomms3325
Article and author information
Author details
Publication history
- Version of Record published: July 3, 2018 (version 1)
Copyright
© 2018, Lewis et al.
This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.
Metrics
-
- 3,065
- Page views
-
- 298
- Downloads
-
- 2
- Citations
Article citation count generated by polling the highest count across the following sources: Crossref, PubMed Central, Scopus.
Download links
Downloads (link to download the article as PDF)
Open citations (links to open the citations from this article in various online reference manager services)
Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)
Further reading
-
- Evolutionary Biology
Understanding how plants adapt to changing environments and the potential contribution of transposable elements (TEs) to this process is a key question in evolutionary genomics. While TEs have recently been put forward as active players in the context of adaptation, few studies have thoroughly investigated their precise role in plant evolution. Here, we used the wild Mediterranean grass Brachypodium distachyon as a model species to identify and quantify the forces acting on TEs during the adaptation of this species to various conditions, across its entire geographic range. Using sequencing data from more than 320 natural B. distachyon accessions and a suite of population genomics approaches, we reveal that putatively adaptive TE polymorphisms are rare in wild B. distachyon populations. After accounting for changes in past TE activity, we show that only a small proportion of TE polymorphisms evolved neutrally (<10%), while the vast majority of them are under moderate purifying selection regardless of their distance to genes. TE polymorphisms should not be ignored when conducting evolutionary studies, as they can be linked to adaptation. However, our study clearly shows that while they have a large potential to cause phenotypic variation in B. distachyon, they are not favored during evolution and adaptation over other types of mutations (such as point mutations) in this species.
-
- Evolutionary Biology
Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.