A New Classification of the Chromodorid Nudibranchs

With over 300 described species, the chromodorid nudibranchs are one of the most species rich families of gastropods.  Their bright colors and interesting morphology appeal to underwater photographers and scientists alike.  Their aposematic coloration has also drawn the attention of scientists interested in natural products chemistry.  In spite of their conspicuousness and appeal, there has been no comprehensive, well-supported phylogeny of the chromodorid nudibranchs.  This hinders progress being made in other biological disciplines where one may assume that species from the same genus represent a monophyletic group.  In a recent issue of PlosOne, Rebecca Johnson and Terrence Gosliner set out to remedy this situation and generate a phylogeny of the chromodorid nudibranchs and present a classification that accurately reflects the evolutionary history of the group.  

In the paper entitled “Traditional Taxonomic Groupings Mask Evolutionary History: A Molecular Phylogeny and New Classification of the Chromodorid Nudibranchs,” Johnson and Gosliner assembled the most comprehensive dataset to date including 244 specimens (142 new), representing 157 species (106 new) chromodorid species and several other taxa.  They used two mitochondrial genes (16S rRNA and cytochrome oxidase I) to reconstruct a phylogeny of the group.  The results revealed that currently recognized genera were either polyphyletic or nested within another genus rendering the other genus paraphyletic.  Extensive homoplasy of morphological attributes that have been thought to be synapomorphies for a particular genus seems to be the cause of the unnatural groupings that have been recognized in the past.  This pattern of polyphyly of recognized genera has been observed for unionid bivalves as well (Campbell et al., 2004).  

One appealing outcome of the study by Johnson and Gosliner (2012) is that they took the time to propose a new classification of the group based on their findings.  As Johnson and Gosliner (2012) indicate, “the translation of phylogenetic hypotheses into classifications is the best way to communicate results to a larger community” and “communicating these new hypotheses is one of the main contributions systematics can make to the scientific community.”  Their study now provides a sound phylogenetic framework from which morphological, chemical and behavioral attributes can be examined.       

Literature Cited

Cambpell, D. C., J. M. Serb, J. E. Buhay, K J. Roe, R. L. Minton, and C. Lydeard.  2005.  Phylogeny of North American amblemines (Bivalvia, Unonoida): prodigious polyphyly proves pervasive across genera.  Invertebrate Biology 124:131-164.

Johnson, R. F., and T. M. Gosliner.  2012.  Traditional taxonomic groupings mask evolutionary history: a molecular phylogeny and new classification of the chromodorid nudibranchs.  PlosOne 7(4):e33479.

Increased Litter Decomposition Rates by Terrestrial Gastropods in Hawaii

Terrestrial gastropods are often a major component of various terrestrial ecosystems.  It is thought that litter-dwelling terrestrial gastropods contribute to the cycling of nutrients either directly or indirectly through metabolism and modifying habitat to enhance micro-arthropod or microbial activity, respectively.  However, their role in ecosystem processes is poorly known particularly in tropical forests.  In a recent issue of Biotropica, Wallace M. Meyer III, Rebecca Ostertag, and Robert H. Cowie shed some light on this very issue in a paper entitled “Influence of Terrestrial Molluscs on Litter Decomposition and Nutrient Release in a Hawaiian Rain Forest.”  Meyer et al. (2013) used a field mesocosm approach to examine (1) whether the presence of terrestrial gastropod species increased rates of leaf litter decomposition, (2) whether different terrestrial gastropod species influence the rates of nutrient release differently, and (3) whether terrestrial gastropods facilitate recruitment of mesoinvertebrates.  The results of the experiments showed that the presence of gastropods increased litter decomposition rates and that the highest decomposition rates were those with the greatest gastropod biomass.  Furthermore, although there were differences in the rates of release of some nutrients among treatments, the different gastropod species appeared to influence nutrient release in a similar way.  Finally, there was no evidence that terrestrial gastropods facilitated mesoinvertebrate recruitment.

The authors have shown empirically that terrestrial gastropods can play a major role in litter decomposition.  One interesting aspect of the study is that it was done using the five most abundant species of gastropods in the Hawaiian rain forest: the native Succinea cepulla and four non-native species (Arion intermedius, Deroceras leave, Oxychilus alliarius, and Limax maximus).    The native species had the lowest density among the gastropods studies and is comparatively rare.  Indeed, Hawaii presents a particularly compelling case because some 65-90 percent of the 750+ species (over 99% endemic) are now considered extinct (Solem, 1990; Cowie et al. 1995; Cowie, 2001; Lydeard et al., 2004) so there is the distinct possibility that invasive gastropod species are now conducting important ecological processes that were once carried out by native species and potentially benefitting otherwise native ecosystems.  Regrettably, important information is lacking to fully address this issue such as species richness and densities in historical, native communities.

Literature Cited

Cowie, R. H., N. L. Evenhuis, and C. C. Christensen.  1995.  Catalog of the native aland and freshwater molluscs of the Hawaiian Islands.  Backhuys Publishers, Leiden, The Netherlands.

Cowie, R. H.  2001.  Invertebrate invasions on Pacific islands and the replacement of unique native faunas: a synthesis of land and freshwater snails.  Biol. Invasions 3:119-136.

Meyer III, W. M., R. Ostertag, and R. Cowie.  2013.  Influence of terrestrial molluscs on litter decomposition and nutrient release in a Hawaiian rain forest.  Biotropica 45(6):719-727.

Lydeard, C., R. H. Cowie, W. F. Ponder, A. E. Bogan., P. Bouchet, S. A. Clark, K. S. Cummings, T. J. Frest, O. Gargominy, D. G. Herbert, R. Hershler, K. E. Perez, B. Roth, M. Seddon, E. E. Strong, and F. G. Thompson.  2004.  The global decline of nonmarine mollusks.  Bioscience 54:321-330.

Solem, A.  1990.  How many Hawaiian land snail species are left? And what we can do for them.  Bishop Museum of Occasional Papers 30:27-40.

Great Unanswered Questions Continued - Deep Molluscan Phylogenetics

The January 2013 issue of American Malacological Bulletin included eight papers from 11 presentations from the James H. Lee symposium, “Great Unanswered Questions in Malacology,” which was held at the 77^th Annual American Malacological Society meeting in Pittsburgh, Pennsylvania, July 23-27 2011.  The organizers, Timothy Pearce and Charles Sturm, introduced each paper (Pearce and Sturm, 2013).  I highlighted one paper previously in my April blog posting, but one that I would like to highlight further as the topic for this blog posting is entitled “Recent advances and unanswered questions in deep molluscan phylogenetics” by Kevin M. Kocot (Kocot, 2013).  Kocot provides a terrific brief review of the leading hypotheses of molluscan phylogeny that have been proposed based on morphological and sequence data such as nuclear small subunit (SSU or 18S) and large subunit (LSU or 28S) ribosomal gene sequences.  Many of these hypotheses have been debated about over many years with each hypothesis having a leading advocate or group of advocates supporting them.  Regrettably, molecular sequence data, which often provides useful data when morphology conflicts offered little information to resolve any of the conflicts and often resulted in bizarre findings such as the lack of monophyly of the Bivalvia and Gastropoda or a paraphyletic Mollusca.  Recently, with the development of phylogenomics, large amounts of nuclear protein-coding gene data derived from genomes and transcriptome data instead of PCR to amplify targeted gene fragments has been generated and found useful in examining the relationships of animals.  In 2011, two papers were published applying phylogenomics to the test of examining deep molluscan relationships (Kocot et al. 2011, Smith et al., 2011) and one examined PCR-amplified regions of seven genes in a target-gene approach (Vinther et al. 2011).  

A consensus tree based on the findings of the three studies was provided as follows:  (((Gastropoda, Bivalvia, Scaphopoda)(Cephalopoda, Monoplacophora))(Polyplacophora,(Neomeniomorpha, Chaetodermomorpha))).  Unlike some previous hypotheses, it is evident that the Aplacophora is monophyletic and sister to Polyplacophora rather than being a paraphyletic grade that was basal and plesiomorphic.  This finding alters our notion of character states for an hypothetical ancestral mollusk.  Also, there is no support for the recognition of the Cyrtosoma (Gastropoda + Cephalopoda), which alters our notion from a comparative framework for those interested in neurobiology of Cephalopods, which may actually be sister to Monoplacophora (although Monoplacophora was only examined in one of the three studies – Smith et al., 2011).

The fact that there was general agreement among the three studies is comforting and leads one to think perhaps we are making progress towards understanding deep phylogenetic relationships of the Mollusca, but many more molecular studies need to be done and sample sizes increased to determine whether the consensus tree will stand the test of time.  Also, in addition to molecular sequence data, as Kocot concludes “more traditional morphological and developmental studies will undoubtedly continue to improve understanding of molluscan evolution while simultaneously raising new questions about this fascinating group of animals.”   

Literature Cited

Kocot, K. M.  2013.  Recent advances and unanswered questions in deep molluscan phylogenetics.  American Malacological Bulletin 31(1):195-208.

Kocot, K. M., J. T. Cannon, C. Todt, M. R. Citarella, A. B. Kohn, A. Meyer, S. R. Santos, C. Schander, L. L. Moroz, B. Lieb, and K. M. Halanych.  2011.  Phylogenomics reveals deep molluscan relationships.  Nature 477:452-456.

Pearce, T. A. and C. F. Sturm.  2013.  Introduction to the James H. Lee symposiu, “Great Unanswered Questions in Malacology,” 77^th annual meeting of the American Malacological Society.  American Malacological Bulletin 31:105-107.

 Smith, S. A., N. G. Wilson, F. E. Goetz, C. Feehery, S. C. S. Andrade, G. W. Rouse, G. Giribet, and C. W. Dunn.  2011.  Resolving the evolutionary relationships of molluscs with phylogenomic tools.  Nature 480:364-367.

Vinther, J. , E. A. Sperling, D. E. G. Briggs, and K. J. Peterson.  2011.  A molecular palaeobiological hypothsis of the origin of aplacophoran molluscs and their derivation from chiton-like ancestors.  Proc. Of the Royal Society B: Biol. Sciences 279:1259-1268.

Ancient Human-Mediated Dispersal of Terrestrial Gastropods

Cepaea nemoralis by L. Holden

                Species have been accidentally or purposely disseminated by humans at an alarming rate over the past century.  Most people have heard about relatively recent invasions and impacts of zebra mussels, Africanized bees, kudzu and other non-indigenous, exotic, or non-native species to name a few.  What many people may not realize is that the true globalization and homogenization of the world’s biota began in 1492 after the “discovery” of the New World by Columbus.  After Columbus, ecosystems met and mixed in an exchange Alfred Crosby referred to as the Columbian Exchange (Mann, 2011).  The “exchange took corn (maize) to Africa and sweet potatoes to East Asia, horses and apples to the Americas, and rhubarb and eucalyptus to Europe- and also swapped about a host of less-familiar organisms like insects, grasses, bacteria, and viruses” (Mann, 2011).  The Columbian exchange had a profound effect on the natural ecosystems and landscapes around the world.  Exotic species became major staple crops that most people do not realize are non-native.  They are here.  We grow them, we eat them or pet them or ride them.  Even fewer people are aware that species were introduced accidentally or purposely thousands of years ago by humans – including terrestrial gastropods!

                In June 2013, Adele Grindon and Angus Davison published a paper in PLOS ONE showing that a peculiar distribution pattern of Cepaea nemoralis land snails in Ireland and the Eastern Pyrenees was best explained by transportation by Mesolithic humans over 8000 years ago.  Apparently, there are a number of species including the Kerry slug, the Pyrenean glass snail and the strawberry tree that are found exclusively in Ireland and Iberia.  This distribution pattern has been referred to as ‘Lusitanian’ and has defied any single explanation.  Grindon and Davison chose to study C. nemoralis because on the West coast of Ireland, C. nemoralis has a large, white-lipped morph that is common and also found in the Pyrenees suggesting some connection that warrants investigation.  The researchers sampled across Europe including Ireland, Britain, northern Spain, southern France and the Pyrenees and sequenced two mitochondrial gene fragments (cytochrome oxidase subunit I (COI) and 16S rRNA) to estimate phylogenies and examine the resultant patterns.  What Grindon and Davison observed was that individuals from Ireland had a mitochondrial lineage, C, that is shared with Central and Eastern Pyrenean populations.  This lineage was absent in most other parts of Europe with minor exceptions.  The authors propose that the best explanation for the disjunct distribution pattern is a single historic long distance dispersal event between the Pyrenees and Ireland.  The species has apparently been a food source in the Pyrenees, so may have been transported live to serve as a source of food.  Grindon and Davison’s paper is not the first documentation of likely human-mediated dispersal of terrestrial gastropods.  Jesse et al. (2011) hypothesized that Neolithic expansion in the western Mediterranean resulted in the expansion of the range of Tudorella sulcata s. str. and Lee et al. (2007) hypothesized pre-historic inter-island introductions of an endemic Pacific island tree snail, Partula hyalina.  It is certain that as other unusual distribution patterns are examined other ancient human-mediated dispersal events will be discovered and shed light on the history of world’s biota including gastropods.  

LITERATURE CITED

Grindon, A. J. and A. Davison.  2011.  Irish Cepaea nemoralis land snails have a cryptic Franco-Iberian origin that is most easily explained by the movements of Mesolithic humans.  PLOS ONE 8(6):1-7.

Jesse, R., E. Vela, and M. Pfenninger.  2011.  Phylogeography of a land snail suggests trans-Mediterranean Neolithic transport.  PLOS ONE 6(6):1-7.

Lee, T., J. B. Burch, T. Coote, B. Fontaine, O. Gargominy, P. Pearce-Kelly, and D. O. Foighill.  2007.  Prehistoric inter-archipelago trading of Polynesian tree snails leaves a conservation legacy.  Proceedings of the Royal Society B 274:2907-2914.

Mann, C. C.  2011.  1493: Uncovering the New World Columbus Created.  Vintage Books, New York.