by Tauana Junqueira Cunha
If we could travel back in time 540 million years, what would the first animals look like? This is one of the longstanding questions scientists aim to answer in the study of how animals evolved and became distinct from their unicellular relatives. To answer it, we need to know how modern animals are related to each other, what order they appeared in, and what evolutionary changes resulted in the diversity we see today.
The traditional view is that the ancestor of all animals was possibly sponge-like and that it gave rise to two descending branches in the animal tree of life: on one side sponges (Fig. 1A) and on the other, a branch that later gave rise to all other animals (see Fig. 2B). However, in 2008, a group of scientists proposed a controversial hypothesis in which comb jellies (Fig. 1B), instead of sponges, were the first branch in the animal tree (see Fig. 2A) . The debate is still ongoing, but research efforts have generated exciting new knowledge about our early origins and about the complexity of animal evolution.
How to build a tree with the evolutionary relationships among animals
When we set out to study relationships among animals, we look for characteristics that are shared due to common history. In the past, external appearance, like body shape, and internal structure, like the presence or absence of cell types, were the only characteristics used to infer relationships. Many of the arguments that favor sponges as the first branch to split in the animal tree are based on this type of evidence: sponges seem to lack some of the complex structures that other animals possess. Nowadays, DNA sequencing enables scientists to compare thousands of genes across animals of interest: closely related animals should have more similar sequences than distantly related ones.
Despite technological advances in DNA sequencing, scientists still have not reached a consensus regarding the earliest relationships in the animal tree. While the comb jelly-first hypothesis has gained strength (Fig. 2A) [2,3], there are still arguments for the traditional sponge-first hypothesis (Fig. 2B) [4,5]. The differences lie in which species or genes are chosen for the analyses and in which methods are used. As our methods for building trees improve, we come closer to finding the final answer.
The hidden biology of sponges and comb jellies
On the bright side, this controversy has helped us understand much more about the ‘hidden’ biology of comb jellies and sponges :
- Getting to know comb jellies: Comb jellies, formally referred to as Ctenophora, are gelatinous marine animals that get their name from eight shiny rows of cilia, called combs, which they use to swim (Fig. 1B, 3A). They live in all parts of the oceans and are voracious predators ! Unlike jellyfish, which swim with their mouth facing down, comb jellies swim with their mouth forward .
Comb jellies have nerve cells, but some of the genes and molecules related to these cells are different from those of other animals. For example, some classical signaling chemicals of other animals, such as acetylcholine (associated with muscular activity), are absent in comb jellies. They can perform similar functions, but in their own unique way .
- Unraveling the complexity in sponges: The group Porifera includes sponges that inhabit all depths of the oceans. They feed by filtering organic particles  from the surrounding water, which they suck inside their body with specialized cells called choanocytes (Fig. 3B). These cells look like the cell of a unicellular organism called choanoflagellate, which is not an animal, but is closely related to them. This superficial similarity made the differences between them go unnoticed for a long time, but a recent comparison elucidated their differences in appearance, function and development . Both kinds of cells have a structure of a collar surrounding a flagellum (a whip-like structure that allows a cell to move), but their shape and the interactions between the two components are distinct (Fig. 3C) , indicating they might have evolved independently in both organisms.
Although some complex traits are indeed absent in sponges, like a nervous system, recent analyses show that their gene composition is similar to that of other animals, including genes related to such complex traits . At the same time, new complex features of sponges are being discovered, like their ability to ‘sneeze’ , which illustrates sensory functions.
Complexity in early animal evolution
The similarity between cells of sponges and cells of non-animals, and the apparent lack of structural complexity in sponges led scientists to two ideas: that sponges were the first group to separate from other animals and that the ancestor of all animals was simple in structure and possibly had a similar cell type. However, if comb jellies were the first animal group to split at the base of the tree, then some of the characteristics that we thought evolved later might have already been present in the first animals. A good example is the nervous system. Because it is absent in sponges, we historically thought that the nervous system had evolved once in the ancestor that gave rise to all of the other animals (Fig. 2). On the other hand, if comb jellies separated first, it means that a nervous system either evolved twice, in comb jellies and other animals excluding sponges, or that sponges lost it during their evolution (Fig. 2). Either way, this scenario implies that at least some of the components necessary for a nervous system were already present in the ancestor of all animals.
Regardless of whether sponges or comb jellies are more distantly related to us, this disagreement has sparked an exciting debate about the origins of early animals and the nervous system, and about patterns of complexity in sponges and comb jellies. Importantly, this debate has shown that we should not think of evolution as a ladder-like process in which complexity grows in one direction, from simpler to more complex animals. Complexity does not run in a single axis, and simple and complex traits are present in every organism.
Tauana Junqueira Cunha is a PhD student in the Department of Organismic and Evolutionary Biology at Harvard University.
 Dunn, C.W. et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452, 745–9. http://www.nature.com/nature/journal/v452/n7188/abs/nature06614.html
 Moroz, L.L. et al. (2014) The ctenophore genome and the evolutionary origins of neural systems. Nature 510, 109–14. http://www.nature.com/nature/journal/v510/n7503/full/nature13400.html
 Borowiec, M.L. et al. (2015) Extracting phylogenetic signal and accounting for bias in whole-genome data sets supports the Ctenophora as sister to remaining Metazoa. BMC Genomics 16, 987. http://bmcgenomics.biomedcentral.com/articles/10.1186/s12864-015-2146-4
 Phys.org (2015) Which came first—the sponge or the comb jelly? http://phys.org/news/2015-12-firstthe-sponge-jelly.html
 Pisani, D. et al. (2015) Genomic data do not support comb jellies as the sister group to all other animals. Proc. Natl. Acad. Sci. 112, 15402–07. http://www.pnas.org/content/112/50/15402.abstract
 Dunn, C.W. et al. (2015) The hidden biology of sponges and ctenophores. Trends Ecol. Evol. 30, 282–91. http://www.cell.com/trends/ecology-evolution/abstract/S0169-5347(15)00062-2
 Migotto, A. (2015) Swallowed Whole – a comb jelly preying on a comb jelly. https://www.youtube.com/watch?v=MmoChWQ6xCk
 Jonathan Bird’s Blue World (2014) Sponges! https://www.youtube.com/watch?v=m8a0oNsDEx8
 Mah, J.L. et al. (2014) Choanoflagellate and choanocyte collar-flagellar systems and the assumption of homology. Evol. Dev. 16, 25–37. http://onlinelibrary.wiley.com/doi/10.1111/ede.12060/abstract
 Riesgo, A. et al. (2014) The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. Mol. Biol. Evol. 31, 1102–20. http://mbe.oxfordjournals.org/content/31/5/1102
 Popular Science (2014) Sponges can sneeze, may have new sensory organ. http://www.popsci.com/article/science/sponges-can-sneeze-may-have-new-sensory-organ
 Brusca and Brusca (2003) Invertebrates, Second Edition, Sinauer Associates, Inc.