Saturday, August 25, 2012

The Enigmatic Pygmy Sunfishes Fishes Find a Phylogenetic Home


Earlier this year my colleagues (Mike Sandel, Kristen Kuhn, Peter Unmack, Peter Wainwright, and Leo Smith), and I published a molecular phylogenetic analysis that resolved Elassoma and Centrarchidae (sunfishes and blackbasses) as a monophyletic group. We used the phylogenetic resolution supported in our analyses to propose that Elassoma be classified in Centrarchidae (1).

Elassoma, or pygmy sunfishes, is a strange group of seven small fish species. All species of Elassoma are endemic to North America and the group is distributed from the south Atlantic Costal Plain through Florida and along the Gulf Coast to Texas, and extend as far north as southern Illinois. Species of Elassoma occupy slow-moving portions of rivers or swamps with ample aquatic vegetation. They are small in size, never exceeding 4 cm in length. While you are not likely to find species of Elassoma in your local pet shop, they are kept in captivity by fish hobbyists where their small size, beautiful colors, and interesting behaviors contribute to their reputation as very fine species to keep in aquaria. Some species of Elassoma are under threat because of impacts on their habitats from human activities, and in particular the Spring Pygmy Sunfish, Elassoma alabamae, has generated much attention from fish biologists as the chances for this species’ survival is, at best, uncertain.

There are many interesting aspects of the biology of Elassoma that evade any comparative study with other percomorph lineages because hypotheses on their phylogenetic relationships have been in dramatic flux since the first species, E. zonatum, was described by David Starr Jordan in 1877 (2). It can be said that Elassoma is probably the most well known of the phylogenetic vagabonds among percomorph fishes, as they have bounced amongst Cichlidae, Centrarchidae (sunfishes and blackbasses), and the inclusive group Smegmamorpha. Despite these very different classifications for Elassoma, from the time of the late 19th Century until the early 1960s they were classified by some ichthyologists as centrarchids, but today they are classified as the only genus in the family, Elassomatidae.

In a landmark study of percomorph phylogeny, Johnson & Patterson proposed that Elassoma, Synbranchiformes (swamp eels), Mugiliformes (mullets), Gasterosteidae (sticklebacks), Syngnathiformes (seahorses), and Atherinomorpha (silversides, halfbeaks, ricefishes, and killifishes) all shared common ancestry based primarily on a single morphological character associated with the backbone (3), specifically the first epineural inserting on a parapophysis or lateral process of its centrum. They named this large inclusive lineage Smegmamorpha. Despite being listed as a group in one of the latest proposed classification of teleost fishes (4), no published phylogenetic analysis of morphological or molecular characters have supported the monophyly of Smegmamorpha (e.g., 5, 6).

It is interesting that three molecular phylogenetic studies using either mtDNA or nuclear genes have resulted in the resolution of a clade containing Elassoma and Centrarchidae (7-9), which harkens back to earlier classifications that considered Elassoma a lineage of centrarchids.

We were motivated to test-drive a set of nuclear genes, several of which we are using for phylogenetic analyses across the entire diversity of ray-finned fishes, to see if they provide ample phylogenetic resolution in percomorphs. In addition, we were motivated to investigate the monophyly of Smegmamorpha and determine the phylogenetic affinities of Elassoma.

Our phylogenetic analyses provide two important results and motivated suggestions regarding the classification of percomorphs. First, Smegmamorpha is not monophyletic and the constituent lineages are distributed among at least four distinct percomorph clades (in the tree figure all sampled Smegmamorpha are highlighted with red branches). We suggest that the continued recognition of Smegmamorpha is unwarranted and the grouping should not be used in subsequent classifications of teleost fishes. Second, the molecular phylogeny resolves a strongly supported clade containing Elassoma and Centrarchidae. The Elassoma-Centrarchidae clade is also resolved in gene trees inferred independently from 9 of the 10 genes. In the paper, we propose that Elassoma be classified along with the sunfishes, blackbasses, rockbasses, and crappies in Centrarchidae.

So why change the family-level classification of Elassoma from Elassomatidae to Centrarchidae? There are two reasons. First, classifying Elassoma as centrarchids communicates that these lineages share common ancestry. Second, the names Elassoma and Elassomatidae are redundant in that they both refer to the same group of species. Some may argue that Elassoma is somehow different enough from all other centrarchids to merit it’s own family. This is a qualitative argument that makes no reference to their phylogenetic relationships, and fails to provide a scientific rationale for maintaining Elassomatidae in the classification of percomorphs.

All phylogenetic hypotheses involve some degree of uncertainty, and being based on inference, rather than deduction, means that we will never know the true phylogeny. We are attempting to reconstruct events that happened long in the hazy past of evolutionary time. Given the caveats of uncertainty in phylogenetic inference, it is my opinion that this paper presents two very strong results that are not likely to change with the addition of more data or increased sampling of percomorph lineages. At the end of the day, it feels quite good to find a nice phylogenetic home for such this charismatic lineage of fishes. 

Note: the very nice picture of Elassoma evergladei was taken by my friend and colleague Noel Burkhead and is on the internet. The map figure was reproduced from Quattro et al (10)

2.  Jordan, D.S. 1877. Contributions to North American ichthyology.  II.  A.-Cottidae, Etheostomatidae, Percidae, Centrarchidae, Aphredoderidae, Umbridae, Esocidae, Dorysomatidae, and Cyprinidae with revisions of genera and descriptions of new or little known species. Bulletin of the United States National Museum. 10:1-68.
3.  Johnson, G.D. and C. Patterson. 1993. Percomorph phylogeny: a survey of acanthomorphs and a new proposal. Bulletin of Marine Science. 52:554-626.
4.  Wiley, E.O. and G.D. Johnson. 2010. A teleost classification based on monophyletic groups, in Origin and phylogenetic interrelationships of teleosts, J.S. Nelson, H.-P. Schultze, and M.V.H. Wilson, Editors. Verlag Dr. Friedrich Pfeil: Munchen. p. 123-182.
5.  Springer, V.G. and T.M. Orrell. 2004. Appendix:  phylogenetic analysis of 147 families of acanthomorph fishes based primarily on dorsal gill-arch muscles and skeleton. - In:  Springer, V.G. & Johnson, G.D. Study of the dorsal gill-arch musculature of teleostome fishes, with special reference to the Actinopterygii. Bulletin of the Biological Society of Washington. 11:236-260.
6.  Detta├», A. and G. Lecointre. 2008. New insights into the organization and evolution of vertebrate IRBP genes and utility of IRBP gene sequences for the phylogenetic study of the Acanthomorpha (Actinopterygii:  Teleostei). Molecular Phylogenetics and Evolution. 48:258-269.
7.  Jones, W.J. and J.M. Quattro. 1999. Phylogenetic affinities of pygmy sunfishes (Elassoma) inferred from mitochondrial DNA sequences. Copeia. 1999:470-474.
8.  Li, B., A. Dettai, C. Cruaud, A. Couloux, M. Desoutter-Meniger, and G. Lecointre. 2009. RNF213, a new nuclear marker for acanthomorph phylogeny. Molecular Phylogenetics and Evolution. 50:345-363.
9.  Santini, F., L.J. Harmon, G. Carnevale, and M.E. Alfaro. 2009. Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishes. BMC Evolutionary Biology. 9:164.
10.  Quattro, J.M., W.J. Jones, J.M. Grady, and F.C. Rohde. 2001. Gene-gene concordance and the phylogenetic relationships among rare and widespread pygmy sunfishes (genus Elassoma). Molecular Phylogenetics and Evolution. 18:217-226.

3 comments:

  1. Mystery solved! Great stuff! So Elassoma is likely to be the sister group to all (other) Centrarchidae? What does Percichthyidae being the sister group to Centrarchidae imply about the origin of Centrarchidae? I bet if an Elassoma were asked, it'd say it's relieved to no longer be a "smegmamorph" Wouldn't you be?

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    1. Aloysius, we actually find that Sinipercidae, is the sister lineage of the Centrarchidae (including Elassoma). However, the Percichthyidae is not far off in the phylogeny. As this part of the Percomorpha phylogeny finds greater resolution, it will be very interesting to investigate the transitions between marine and freshwater habitats in these lineages.

      As for asking Elassoma about Smegmamorpha, well I am going to leave that one to the fishes!

      Thank you for your comment.

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