Convergence of ion channel genome content in early animal evolution

Abstract

Multicellularity has evolved multiple times, but animals are the only multicellular lineage with nervous systems. This fact implies that the origin of nervous systems was an unlikely event, yet recent comparisons among extant taxa suggest that animal nervous systems may have evolved multiple times independently. Here, we use ancestral gene content reconstruction to track the timing of gene family expansions for the major families of ion-channel proteins that drive nervous system function. We find that animals with nervous systems have broadly similar complements of ion-channel types but that these complements likely evolved independently. We also find that ion-channel gene family evolution has included large loss events, two of which were immediately followed by rounds of duplication. Ctenophores, cnidarians, and bilaterians underwent independent bouts of gene expansion in channel families involved in synaptic transmission and action potential shaping. We suggest that expansions of these family types may represent a genomic signature of expanding nervous system complexity. Ancestral nodes in which nervous systems are currently hypothesized to have originated did not experience large expansions, making it difficult to distinguish among competing hypotheses of nervous system origins and suggesting that the origin of nerves was not attended by an immediate burst of complexity. Rather, the evolution of nervous system complexity appears to resemble a slow fuse in stem animals followed by many independent bouts of gene gain and loss.

Keywords: ASIC/ENaC; Cys-loop receptor; ancestral genome reconstruction; ionotropic glutamate receptor; potassium channel.

Fig. 1.

Gain and loss of ion-channel families in opisthokont evolution. The two trees have identical topologies. The branch lengths of the tree on the left are the net gain (gains minus losses), and the branch lengths of the tree on the right represent percent loss (losses minus gains as a percentage of parent copy number). Total numbers of ion channels in each taxon are shown on the left-hand tree. Two branches in animals that had large loss events are labeled: the common ancestors of deuterostomes (1) and of ecdysozoans (2).

Fig. 2.

Ion-channel genome content of internal nodes on the animal phylogeny. Ion-channel families that underwent large expansions are colored green (GIC), burnt orange (K_v), and black (LIC). Voltage-gated sodium channels, which drive action potentials but did not experience duplication events on the same scale, are colored gray. All other families are left blank but are shown for comparison. Branches with many duplications are colored red, and those with net losses are colored blue. Two hypotheses about nervous system origins from the literature are also shown. Open symbols show one hypothesis, which posits one origin (open circle) in the common ancestor of animals and two losses (open cross) in placozoans and sponges (13, 14). Filled circles show an alternative hypothesis that nervous systems have two origins—one in the common ancestor of cnidarians and bilaterians and one in the ctenophore lineage (12, 13, 15, 20). Neither hypothesis corresponds with nodes that have large duplication events.

Fig. 3.

(A) Channel counts of extant species and ancestral species. (B) Species tree showing the relationships of extant taxa and the location of key ancestral nodes. (C) PCA of normalized ion channel gene contents for all tips and three ancestral nodes. Proximity in the space of the two PCs indicates similar gene contents. Loadings of the ion-channel families are shown as vectors in the two axes. The size and direction of the loading vector indicates its correlation with the two components. Loading arrows point to regions where that gene family is in high relative abundance. Labeled species are Amphimedon (Aq) and Ciona (Ci).