Barnacle Evolution: A Tribute to Alan J. Southward (1928-2007)

Its a brand new year! Thats means I get to have 2008 in my Endnote catalogue! So what was the first paper of the year that I downloaded?

Perez-Losada, M., M. Harp, J. T. Hoeg, Y. Achituv, D. Jones, H. Watanabe, and K. A. Crandall. 2008. The tempo and mode of barnacle evolution. Molecular Phylogenetics and Evolution 46:328-346.

This was tempered by the news of the passing of one the world's great barnacle biologists, Alan J. Southward. I never got a chance to meet him, though I heard from several people he was great guy. The Liverpool Daily Post's obituary gives a brief example:

"At a more homely level, he was a kind and humorous man, white-haired and bushy-browed, who devoted his immense intellect to discovering more about simple creatures, which, though unseen and unsung, experience the precious gift of life on Earth."

But I have gotten known his research since 2003 when I became interested in stalked barnacles from hydrothermal vents at the East Pacific Rise. Relishing an opportunity to go on board a research expedition with a boat full of taxonomists (though I came with a small geology contingent), I saw for the first time in my life the stalked barnacle, Neolepas zevinae. Barnacles on stalks were a new concept for me. N. zevinae was described in 1979 by Bill Newman from Scripp's Institute for Oceanography. He is still alive and was a colleague of Dr. Southward. The poster below describes them well (from a newspaper by Sam Hinton in 1981).

Alan Southward was more than just a barnacle biologist. Like Charles Darwin, the foremost authority on barnacles, Dr. Southward studied biogeographic patterns and isolating barriers using barnacle distributions. He studied the damage to the marine ecosystem by pollutants in the 1950s, showing how long it took for ecosystems to recover. Additionally, he was one of the first to study the effects of environmental temperature increases on marine invertebrate fauna, way before global warming was a hotbed issue. Alan Southward worked with other marine organisms, most notably Pogonophorans, but limpets and fish as well as being an accomplished marine biologist. He worked 19 beyond his retirement, focusing heavily on hydrothermal vent organisms.

For further information about this naturalist who exemplified a lifetime of learning, I encourage you to look up his publications. I'm happy to provide some from my personal library too! Paul Dando, a researcher at the Marine Biological Station who worked with Dr. Southward, wrote an excellent obituary article in this week's Nature. It is well worth the read. With that being said, this post on barnacle evolution is dedicated to the memory of Alan J. Southward. Cheers!
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Lepas anatifera from Washington state, USA. Photo credit: David Cowles 1997.

Perez-Losada et al. (2008) published a MEGA barnacle data set using 3 nuclear genes and 44 morphological characters for 91 taxa in the superorders Thoracica and Rhizocephala. They rewrote barnacle evolution by rejecting some of the hypotheses that were the foundation for barnacle biology and systematic, while giving statistical and phylogenetic support for others and creating new hypotheses. This study forms the new basis for understanding barnacle evolution and basic biology. This has many implications for other fields. In particular, barnacles are the marine industry's most wanted. They foul docks, boats, and anything else with a part in the seawater, including other animals! Whales, sea turtles, other crustaceans and just about anything else can become a barnacle colonization substrate.

Though Linnaeus, and/or his students, certainly described barnacles, the real authority was Charles Darwin. He spent over 8 years cataloging, describing and monographing every barnacle he could get his hands on from every part of the world. This resulted in 4 comprehensive tomes that are still referenced and cited today. Darwin Online has the complete works freely available over the internet: Living Cirripedia Volumes 1 & 2 and Fossil Cirripedia of Great Britain Volumes 1 & 2. Darwin based much of his taxonomy on shell characteristics, though he certainly studied the internal "soft" parts.

The cirripede shell is formed by plates secreted by the cuticle. They are not molted, or shed, like in other arthropods but increase in size circumferentially and in height. The number of shell plates were traditionally hypothesized to increase from a thoracican ancestor with 4 or 5 plates during the course of evolution. Other groups in the Thoracica with more plates are thus more derived. It is uncertain to what the selective pressure was to develop different numbers of plates. Perhaps more smaller plates offer greater protection than fewer larger plates. What Perez-Losada et al. found out though was there were no clear patterns with plate enumeration. Clades with no plates are mixed in with clades with 5 plates, while a clade with more than 12 plates is sister to a clade with a last common ancestor that had no more than 7 plates. The theory of shell plate evolution is clearly debunked in this analysis, though they can say with some degree of certainty that the last common ancestor to the Thoracica had no more than 4 plates. Another interesting point is that asymmetry (Verrucomorpha) has evolved independently at least twice in the thoracican lineage. I believe this highlights the plasticity in biomineral characters, such as shell characteristics. This is seen in many molluscan clades where general shell characteristics are misleading, sometimes due to external parameters (erosion) and sometimes due to phenotypic plasticity in the mechanisms that construct biomineral structures. Thus, the soft parts and larval characteristics are more important (though often more difficult to study and they leave no fossil trace).

Figure 3 from Perez-Losada et al. (2008): "Thoracican divergence time chronogram estimated using the 50% majority-rule consensus BMCMC tree of morphological and molecular data under mix-models..." See paper for more details.

On a sytematic level they uncovered several polyphyletic clades, such as the Heterlepadomorpha (those that have no shell plates). This clade appears to have evolved at least twice, independently, and in both cases are more derived (within clades that have more than 5 plates) and a more recent radiation. The previously well established clades of the Verrucomorpha, Scalpellomorpha and Sessilia are no more, while the Iblomorpha and Balanomorpha have gained unequivocal support. One grouping that caught my attention is the clade below (magnified from above).


Especially everything under and including the clade marked 'Verrucomorpha (7s)'. All those barnacles - Neoverruca, Ashinkailepas, Vulcanolepas, Leucolepas and the aforementioned Neolepas are - are hydrothermal vent barnacles from the Pacific Ocean. I am very surprised to see this neat and well supported grouping. In particular, the stalked barnacle Vulcanolepas osheai is known the farm chemoautotrophic bacteria on its cirri. The more vent scientists look, the more it seems that vent organisms tend to form clades despite geographic distance, barriers or classical taxonomic ranks. We are seeing similar grouping in anemones, caridean shrimp, bythograeid crabs, and of course all the chemoautotrophic taxa: siboglinid annelids, bathymodiolin mussels, and vesicomyid clams. The habitat appears to be a unifying factor. I wonder what else in this phylogeny groups together by habitat? I know I've found Arcoscapellum sp. hanging off the antenna of an anomuran crab (Eumunida picta), perhaps it is related to other crab hitchhiking barnacles.

This study is a great study for many reasons, partly because it answers some questions, but mostly because it rearranges our thinking about the taxa in question and gives us more avenues to explore. I didn't highlight all the major discoveries from this article, such as the fine-tuning of the tempo of evolution, but I hope to see future papers addressing the evolutionary ecology of barnacles in light of the new systematic rearrangement. Taxonomy is at the point now where they needs to be substantial revolutions to be made in order to progress from stagnancy. This study and others like it using 'total evidence' (i.e. combining morphological characters, life history traits and genetics) will pave the way to understanding animal evolution and give systematics the credit it deserves, both financially and publicly. So cheers Dr. Southward, I'm sure you are resting well in the cirri of your loved organisms.