Monday, September 3, 2012

An Adaptive Radiation on Ice

 In February of 2012 we published a set of comparative analyses to investigate the adaptive radiation of Antarctic notothenioids, a clade of percomorph teleosts. The authors included a graduate student in my lab, Alex Dornburg, a former postdoc, Kristen Kuhn, the venerable master of Antarctic fishes, Joseph T. Eastman, a former Near Lab Yale undergraduate, Jillian Pennington, my valued Italian colleagues, Tomaso Patarnello and Lorenzo Zane, a fish physiologist from Argentina, Daniel A. Fernández, and my oft partner in high seas Southern Ocean mischief, Christopher D. Jones who was our cruise leader.

Artedidraco skottsbergi (9 cm) collected in the Bransfield Strait.
Photograph by Thomas J. Near
Dissostichus mawsoni,
Antarctic Toothfish
The term adaptive radiation has been applied to very few marine fish lineages. The notothenioids exhibit anti-freeze glycoproteins (AFGP) to avoid freezing in the subzero waters of the Southern Ocean around Antarctica. Antarctic notothenioids exhibit substantial morphological and ecological differences among closely related species, ranging from the pelagic Antarctic Toothfish, Dissostichus mawsoni, which can reach 1.75 m in length, to the entirely benthic Artedidraco skottsbergi that has a maximum size of only 11 cm. All notothenioids lack a swim bladder, the primary buoyancy organ of ray-finned fishes and homologous to our lungs; however, several lineages of notothenioids have evolved modifications of buoyancy through reduction of ossification and lipid deposits. Some notothenioids are neutrally buoyant, meaning they have no weight in seawater. The differences in buoyancy among closely related species is nearly as substantial as differences in their morphology.

The field work for this study encompassed four expeditions (2001, 2003, 2006, and 2009) to the Southern Ocean onboard the Russian research vessel Yuzhmogeologia. On these cruises I was able to make buoyancy measurements from more than 1,000 specimens, and I collected more than 2,000 specimens and tissue samples that are now housed in the fish collection of the Peabody Museum of Natural History.

Eleginops maclovinus, the non-Antarctic sister species to the entire notothenioid 
Antarctic Clade. Maximum size is 90 cm.
There are approximately 100 species that comprise an unnamed Antarctic Clade that is considered an adaptive radiation, but there are also three species-poor lineages that are early branching and endemic to non-Antarctic cold-temperate near-shore habitats in South America, Falkland Islands (Islas Malvinas), Tristan de Cunha, Australia, Tasmania, and New Zealand. These lineages include Bovichtidae, Pseudaphritis urvillii, and Eleginops maclovinus. These lineages were never exposed to the freezing conditions of the Southern Ocean and provide an important contrast to understand the origins of the adaptations to polar conditions, as well as the ecological and morphological diversity observed in the Antarctic Clade.
Distribution of Eleginops maclovinus

Previous work that I had published, using relaxed molecular clock analyses of mitochondrial DNA rRNA gene sequences, indicated that the Antarctic Clade originated around 24 mya. This is well after the onset of global cooling and appearance of the first Antarctic ice sheets at the Eocene-Oligocene boundary, some 35 mya. Subsequent molecular age estimates using primarily DNA sequence data from nuclear genes have confirmed this result. However, there was no analysis that assessed if Antarctic notothenioids exhibit an explosive diversification subsequent to their origin, a pattern expected in an adaptive radiation.

My colleagues and I investigated the tempo of diversification in notothenioids through analyses of a time-calibrated phylogeny that was inferred from DNA sequences of five nuclear genes (myh6, sh3px3, tbr1, zic1, and the first intron of the S7 ribosomal protein) and two mitochondrial genes (ND2 and 16S rRNA). The phylogenetic analysis included 83 of the approximately 120 recognized notothenioid species.

The inferred molecular phylogeny is quite orthodox, relative to previous inferences from morphological and molecular data. For example, Bovichtidae (containing Bovichtus and Cottoperca) and Pseudaphritis urvillii are successive early diverging non-Antarctic lineages, and the South American and Falkland Island distributed Eleginops maclovinus (pictured above) is the sister lineage of the Antarctic Clade. Within the Antarctic Clade the only noteworthy result is the paraphyly of Nototheniidae, but support for the inferred relationships among the earliest diverging lineages of the Antarctic Clade is limited.

Estimating the ancestral character states of AFGP on the notothenioid time tree supports a single origin of the trait along the branch subtending the most recent common ancestor of the Antarctic Clade. A method that detects changes in lineage diversification rate identified the Antarctic Clade and the common ancestor of Artedidraconidae, exclusive of Artedidraco skottsbergi, as exhibiting high diversification rates relative to the estimated background diversification rate. However, when we performed additional temporal analyses, it was clear that there are pulses of lineage diversification among much younger lineages in the Antarctic Clade. In other words, a shift of diversification rate leading to the Antarctic Clade is consistent with the expectation that AFGP was a trigger to the notothenioid adaptive radiation, we also observed temporal periods of high diversification that are at least 10 million years after the origin of AFGP. It does not seem that the origin of AFGP tells the whole story of the notothenioid adaptive radiation.

It is important to note that unlike any other set of near-shore marine habitats on Earth, the fish fauna of the Southern Ocean is completely dominated by the closely related notothenioids. This was not always the case. A fossil fish fauna from Seymour Island at the tip of the Antarctic Peninsula clearly shows that about 40 mya Antarctica was the home of a temperate and phylogenetically diverse teleost fauna that was not much different from what I can see off shore from New Haven in Long Island Sound. As polar conditions developed in the Southern Ocean this fauna was extirpated, opening up a set of niches that were ultimately exploited by notothenioids. In this paper we propose that the particularly harsh environmental and physical conditions of near-shore habitats in Antarctica, particularly starting about 14 mya, may have led to a cycle of lineage extirpation, recolonization, and diversification within the notothenioid Antarctic Clade. This hypothesis is supported by our finding of pulses of diversification associated with the most species-rich notothenioid lineages (e.g., Artedidraconidae, Trematomus, and Channichthyidae) that correspond to a time around 10 to 5 mya.

Vomeridens infuscipinnis, a species of Bathydraconidae, or dragonfishes.
This species is very light in water, with the lowest buoyancy among measured
bathydraconids. Photograph by Thomas J. Near
Trematomus newnesi, a semi-pelagic species of Nototheniidae
that has an intermediate buoyancy. Photograph by Thomas J. Near
When we examined the pattern of diversification of buoyancy in notothenioids, there is a clear pattern of substantial among clade disparity early in the diversification of the Antarctic Clade, just as expected in an adaptive radiation. However, two of the most species-rich notothenioid subclades, Channichthyidae and Trematomus, show substantial within lineage disparity throughout their respective histories. This indicates that unlike the Antarctic Clade as a whole, closely related species in these lineages are evolving substantial differences in buoyancy.

In this paper we pointed out that regions of the Southern Ocean are among the fastest warming regions on Earth. Such dramatic thermal changes may be cause for concern when considering the future of these cold-adapted fishes. From the perspective of studying the notothenioid adaptive radiation, future work should aim to provide greater phylogenetic resolution among the early diverging lineages of the Antarctic Clade, assess the relationships between habitat and dietary resource utilization, and continue to refine our understanding of species diversity in the clade. Notothenioids are a most fascinating lineage of animals and the fact they are fishes just adds that much to their allure and ensures that we will be paying attention to them for the foreseeable future.

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