Convergence part 6: the deepest of deep homologies

You are more closely related to a mushroom than a kelp is to a plant. It’s strange to think about, but it’s true. Kelps seem very plant-like, with their root-like holdfasts, stalk-like stipes, and leaf-like blades. But kelps are brown algae, part of the stramenopile (or heterokont) lineage of eukaryotes, which are very distant from the land plants and their green algal relatives, all of which are within the archaeplastida (the direct descendants of the primary origin of chloroplasts). Mushrooms (fungi) and humans (animals), on the other hand, are both opisthokonts, practically cousins at the scale we’re talking about.

Pawlowski 2013 Fig. 1

Figure 1 from Pawlowski 2013. Deep phylogeny of eukaryotes showing the position of small eukaryotic lineages that branch outside the seven supergroups (modified after Burki et al. 2009; drawings S Chraiti). You are represented by a fish, which at this scale you might as well be.

Molecular clocks estimate the divergence between animals and fungi on the order of a billion years ago, with some estimates ranging as high as 1.5 billion. Estimates for the split between stramenopiles and archaeplastida tend to be about a half billion years older (for example, 1.55 versus 1.96 billion in Hedges et al. 2004, 1.30 versus 1.78 billion in Parfrey et al. 2011). Our minds have a tendency to compress very old timespans, so let me point out that that half billion year difference is about the same amount of time that has passed between the end of the Cambrian and the present. Give or take a few tens of millions of years.

In parts one through five of this series, I refuted the revisionist history some intelligent design advocates have created, in which evolutionary biologists have only recently learned about widespread convergence. I also argued that widespread convergence does not undermine common descent, as some in that community have claimed. This post was going to be about convergence in Volvox, and I promise I’ll get to that. I got sidetracked, though, by a new preprint by Alok Arun and colleagues, “Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups.” Since it relates to both convergence and algae, I couldn’t pass it up.

Arun and colleagues show that two transcription factors, Ouroboros and Samsara, are involved in life cycle regulation in the model brown alga Ectocarpus. Mutations in either gene convert the sporophyte generation into a gametophyte:

Arun et al. 2018 Fig. 1A

Figure 1A from Arun et al. 2018. Life cycle of wild type and oro mutant Ectocarpus. The wild type sexual cycle (upper panel) involves production of meio-spores by the diploid sporophyte via meiosis in unilocular (single-chambered) sporangia (US). The meio-spores develop as haploid, dioecious (male and female) gametophytes. The gametophytes produce gametes in plurilocular gametangia (PG), which fuse to produce a diploid sporophyte. Gametes that fail to fuse can develop parthenogenetically to produce a partheno-sporophyte, which can produce spores by apomeiosis or following endoreduplication to engender a new  generation of gametophytes. PS, plurilocular sporangium (asexual reproduction). Gametes of the oro mutant (lower panel) are unable to initiate the sporophyte program and develop parthenogenetically to produce partheno-gametophytes. The mutation is recessive so a cross with a wild type gametophyte produces diploid sporophytes with a wild type phenotype.

The basic eukaryotic life cycle alternates between fusion of two haploid cells (fertilization) and reduction division of a diploid cell into four haploid cells (meiosis). One or the other or both phases reproduce asexually through mitosis to produce cells of the same ploidy, and sometimes these cells remain attached to form a multicellular body. In animals, for example, mitosis occurs in the diploid phase, and the resulting diploid cells stay together (to use Corina Tarnita’s terminology) to form the multicellular body. In the volvocine algae, mitosis occurs in the haploid phase, and the resulting haploid cells stay together to form the multicellular body.

In Ectocarpus, mitosis occurs in both the haploid and the diploid phase, and multicellular bodies (or thalli) are formed in both phases. Two haploid gametes fuse to form a diploid zygote that develops through mitosis into a sporophyte. The sporophyte produces haploid meio-spores through meiosis, and these develop (again through mitosis) into gametophytes. All of this is shown on the left-hand side of Figure 1A above, the Sexual cycle. Another possibility exists for gametes, though: gametes that fail to find a mate can develop directly into a multicellular partheno-sporophyte, which produces haploid spores capable of developing into gametophytes. Mutations in Ouroboros or Samsara disrupt this process, leading unmated gametes to develop into gametophytes instead of partheno-sporophytes.

What’s amazing about this is that genes from the same family do something very similar in land plants. Ouroboros and Samsara are both three amino acid loop extension homeodomain transcription factors (TALE HD TFs). Two TALE HD TFs, MKN1 and MKN6, are involved in life cycle regulation in the moss Physcomitrella patens, and loss of function mutations in these genes have the same effect as in Ectocarpus: conversion of the sporophyte generation into a gametophyte.

One of the most surprising outcomes that began to emerge in the 1990s from comparative studies of developmental genetics was that similar genes sometimes control the development of body parts in distantly related species, even when the ancestor of those species lacked similar structures. For example, similar genes control the development of paired appendages in vertebrates and in arthropods, even though the most recent common ancestor of vertebrates and arthropods didn’t have paired appendages. Similarly, some of the same genes control the development of camera-type eyes in vertebrates and cephalopods, even though the most recent common ancestor of vertebrates and mollusks didn’t have eyes.

This pattern is called “deep homology,” and it suggests that the same or similar genes were independently recruited for similar purposes in separate lineages. The discovery that similar genes control the gametophyte to sporophyte transition in land plants and brown algae is a spectacular example of deep homology. The lineages that led to land plants and brown algae diverged over 1.5 billion years ago, and both lineages remained unicellular for hundreds of millions of years after that. Yet each lineage eventually evolved a complex multicellular life cycle, and they used some of the same genes to do so. This is the deepest example of deep homology that I have heard of.

Arun and colleagues conclude,

The recruitment of TALE HD TFs as sporophyte program master regulators in both the brown and green lineages represents a particularly interesting example of latent homology, where the shared ancestral genetic toolkit constrains the evolutionary process in two diverging lineages leading to convergent evolution of similar regulatory systems (Nagy et al., 2014). The identification of such constraints through comparative analysis of independent complex multicellular lineages provides important insights into the evolutionary processes underlying the emergence of complex multicellularity. One particularly interesting outstanding question is whether HD TFs also play a role in coordinating life cycle progression and development in animals? Analysis of the functions of TALE HD TFs in unicellular relatives of animals may help provide some insights into this question.


Stable links:

Arun, A., S. M. Coelho, A. F. Peters, S. Bourdareau, L. Pérès, D. Scornet, M. Strittmatter, A. P. Lipinska, H. Yao, O. Godfroy, G. Montecinos, K. Avia, N. Macaisne, C. Troadec, A. Bendahmane, and J. M. Cock. 2018. Convergent recruitment of life cycle regulators to direct sporophyte development in two eukaryotic supergroups. bioRxiv 460436. DOI: 10.1101/460436

Burki, F., N. Okamoto, J. F. Pombert, and P. J. Keeling. 2012. The evolutionary history of haptophytes and cryptophytes: Phylogenomic evidence for separate origins. Proc. R. Soc. B Biol. Sci. 279:2246–2254. DOI: 10.1098/rspb.2011.2301

Hedges, S. B., J. E. Blair, M. L. Venturi, and J. L. Shoe. 2004. A molecular timescale of eukaryote evolution and the rise of complex multicellular life. BMC Evol. Biol. 4:2. DOI: 10.1186/1471-2148-4-2

Nagy, L. G., R. A. Ohm, G. M. Kovács, D. Floudas, R. Riley, A. Gácser, M. Sipiczki, J. M. Davis, S. L. Doty, G. S. De Hoog, B. F. Lang, J. W. Spatafora, F. M. Martin, I. V. Grigoriev, and D. S. Hibbett. 2014. Latent homology and convergent regulatory evolution underlies the repeated emergence of yeasts. Nat. Commun. 5471. DOI: 10.1038/ncomms5471

Parfrey, L. W., D. J. G. Lahr, A. H. Knoll, and L. A. Katz. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc. Natl. Acad. Sci. U.S.A. 108:13624–9. DOI: 10.1073/pnas.1110633108

Pawlowski, J. 2013. The new micro-kingdoms of eukaryotes. BMC Biol. 11:40. DOI: 10.1186/1741-7007-11-40

Tarnita, C. E., C. H. Taubes, and M. A. Nowak. 2013. Evolutionary construction by staying together and coming together. J. Theor. Biol. 320:10–22. DOI: 10.1016/j.jtbi.2012.11.022


Leave a Reply