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.    

On the diversity of land snails Down Under

By Frank Köhler
Australian Museum, 6 College Street, Sydney NSW 2010, Australia
    
     Ever since Europeans have set foot here, Australia has been a pretty exciting place for biologists. While the first reports on hopping creatures and duck billed water moles were initially met with suspicion back in Old Europe, it soon became clear that the continent indeed harbours a unique fauna and flora, which resembled little the biotas found elsewhere in the world. And because the place is big, there has been a lot to discover – and trust me, there still is. In fact, it is estimated that Australia is home to about 600,000 native species of plants and animals, or in other terms, perhaps 10 per cent of Earth’s biodiversity. However, you may be surprised to learn that a whopping three quarters of these species are awaiting discovery. On the other hand, Australia has also suffered the largest documented decline in biodiversity of any continent over the last 200 years due to the grave impact of humans on the natural world. As a result, Australia ranks high amongst the global hotspots of endangered and extinct species (Department of Environment, 2009).

Amplirhagada boongareensis

     If we seriously want to stop or at least slow down the current rate of species loss, we need to better understand how Australian biodiversity is made up, how it is distributed throughout the continent, and which are the main factors that cause the decline and ultimately extinction of species. Only then can we develop appropriate conservation strategies that meet the urgency of the case. Frankly, this seems to be an awful lot of work. While it is utterly unrealistic to hope we could gain adequate knowledge of all groups of organisms at once, focussing on a number of model groups might be the one way to go. Such model groups would then serve as surrogates for ‘the other 99% of biodiversity’ as so dubbed by Ponder & Lunney (1999). And that is where land snails come into play. A number of factors render land snails promising model organisms for conservation related research. Firstly, Australian land snails display exceptionally high levels of endemism, which in fact exceed levels found in most other faunal groups. About 98.6% of all native species are endemic to Australia (that is, they occur nowhere else) (Slatyer et al., 2007). Moreover, marked endemism is found on much finer spatial scales, with some species having extremely small ranges of a few square kilometres. This endemism is tightly correlated with low mobility and acute moisture sensitivity of the organisms – a combination that renders snails susceptible to changes in their habitat, be it due to climate change or more direct and localized disturbances from urban development, mining, oil and gas exploration or other forms of land use.

     Exactly for these reasons, land snails are increasingly targeted in biological surveys and used to monitor the effects of landscape degradation, environmental change or to evaluate the conservation significance of certain areas. For example, land snails were the only invertebrate group surveyed in the Kimberley Island Survey, during which between 2008 and the little known biota of islands off the remote north-western Australian coast was surveyed. This project gathered new records of endangered vertebrates, but most significantly, it also led to the discovery of nearly 100 new species and five new genera of land snails (Kimberley Island Survey). This brings us to another favourable aspect of land snails: Their taxonomic and ecological diversity. Briefly, snails are diverse enough to allow meaningful analyses of diversity patterns but are not too diverse, causing ongoing taxonomic nightmares.

     Molluscan studies in Australia look back to nearly 250 years of history. The first species were collected during explorations and voyages along the coastal fringes. Most significantly, the early French voyages to Australia yielded over 50 newly described species (Dance, 1986). These species were often described with dubious or imprecise locality information, which continues to cause taxonomic difficulties and ambiguity until today (e.g.,  Köhler, 2012). From 1850 on, when the continent became better known and more densely settled, a small but proliferous scene of Australian taxonomists begun to flourish. Within just a hundred years, workers such as James Charles Cox, John William Brazier, Ralph Tate, Charles Hedley and Tom Iredale, together named more than 1,300 species. While these early works were entirely shell-based, the American malacologist Alan Solem initiated the modern era of Australian malacology. In his hallmark work, which incorporated comparative anatomy, particularly genital anatomy, Solem revised the taxonomy of most Western and Central Australian taxa and described hundreds of new species (Cameron et al., 2005).

     Despite the on-going descriptions of new taxa, by end of the millennium the number of recognized species had dropped dramatically to 504 because many previously introduced names were relegated to synonymies (Smith, 1992). However, Slatyer et al. (2007) argued that 2000 was a more realistic estimate for the total number of species throughout Australia. This notion has largely been confirmed recently. In the last five years alone, the number of recognized species increased to about 1,200. This increase results primarily from new descriptions of species but also the removal of names from synonymies in a monograph of the eastern Australian fauna (Stanisic et al., 2010). Accordingly, about 750 species are now documented from the mesic eastern fringes of the continent. In addition, a recent series of taxonomic treatments of north-western Australian camaenids has probably doubled the number of known species from this part of the country approximately 350. 

     Eventually, the current decade has also seen the first more comprehensive molecular phylogenetic studies of Australian land snails. Molecular phylogenetic studies, even though still in their infancies, contributed significantly to disentangle systematic relationships within several main groups, aided the recognition of morphologically cryptic species, and provided intriguing insights into patterns of land snail evolution across Australia (e.g., Hugall & Stanisic, 2011; Criscione et al., 2012; Köhler & Johnson, 2012). We learned that the diversity of land snails throughout Australia is governed mainly by availability of water and complexity of habitat. In addition, factors, such as distribution of surface layers of limestone and historical habitat fragmentation due to increased acidification since the Tertiary have played an important role in lineage diversification by creating faunal refuges both on spatial and temporal scales. These factors shaped the distributions of many taxa, which display recurrent patterns of western vs. eastern, peripheral vs. interior and northern vs. southern distributions. The highest diversity of species is found in the eastern Australian mesic zone, which harbours several major land snail radiations, such as the Camaenidae, Charopidae, Helicarionidae and Rhytididae. Additional hotspots of diversity are found in the Western Australian Kimberley as well as the rocky ranges of Central Australia. These regions, however, boast radiations of only one land snail group, the Camaenidae.

     On-going works continue the taxonomic description of the Australian fauna demonstrating that the process of discovery is far from over. Large efforts are being made to close survey gaps (i.e., by conducting helicopter-based surveys in remote regions) but the vastness and remoteness of the continent and the comparatively small workforce of taxonomists set limits to the pace of progress. Our on-going studies are aiming to tie together taxonomic description, phylogenetic inference and collection-based biodiversity analyses in order to gain deeper insights into the evolution of Australian land snails and a more comprehensive understanding of patterns in order to improve current conservation management.

Literature Cited

Australian Government (2013). Conservation of biodiversity. Online resource at http://www.environment.gov.au/biodiversity/index.html (looked up 14 February 2013).

Cameron, R.A.D., Pokryszko, B.M. & Wells, F.E. (2005) Alan Solem's work on the diversity of Australasian land snails: an unfinished project of global significance. Records of the Western Australian Museum Supplement, 68, 1-10.

Criscione, F., Law, M.L. & Köhler, F. (2012) Land snail diversity in the monsoon tropics of Northern Australia: revision of the genus Exiligada Iredale, 1939 (Mollusca: Pulmonata: Camaenidae), with description of 13 new species. Zoological Journal of the Linnean Society, 166, 689-722.

Dance, S.P. (1986) A history of shell collecting. Backhuys/Brill, Leiden.

Department of Environment, W., Heritage and the Arts (2009) Australia’s fourth national report to the UN Convention on Biological Diversity. In, Canberra.

Hugall, A.F. & Stanisic, J. (2011) Beyond the prolegomenon: a molecular phylogeny of the Australian camaenid land snail radiation. Zoological Journal of the Linnean Society, 161, 531-572.

Köhler, F. (2012) Taxonomic revision of two endemic land snail genera from the Top End of Northern Australia with remarks on two problematic species named by de Férussac and Le Guillou (Eupulmonata, Camaenidae). Zoosystematics and Evolution, 88, 53–62.

Köhler, F. & Johnson, M.S. (2012) Species limits in molecular phylogenies: A cautionary tale from Australian land snails (Camaenidae: Amplirhagada). Zoological Journal of the Linnean Society, 165, 337-362.

Slatyer, C., Ponder, W.F., Rosauer, D. & Davis, L. (2007) Between a rock and a dry place – land snails in arid Australia. Animals of arid Australia. Out on their own? (ed. by C. Dickman, D. Lunney and S. Burgin), pp. 30-41. Royal Zoological Society of New South Wales, Mosman, NSW.

Smith, B.J. (1992) Non-marine Mollusca. Zoological Catalogue of Australia (ed. by W.W.K. Houston), pp. 1-408. Australian Government Publishing Service, Canberra.

Stanisic, J., Shea, M., Potter, D. & Griffiths, O. (2010) Australian land snails. Bioculture Press, Riviere des Anguilles, Mauritius.

Does one species of giant squid roam the world’s oceans? Some tantalizing new answers from mtDNA

By Peter Marko
Associate Professor of Biological Sciences and President of the American Malacological Society
Clemson University  (soon moving to University of Hawaii)

We’ve seen a string of recent papers published that support what many biologists and taxonomists have long suspected, that there are many more undescribed species than described species on Earth.  Although indirect estimates are always controversial, it's safe to say that it's going to be a long time before we ever have anything close to a complete list of species for our planet.

Last month, however, that hypothetical list of species may have gotten a little bit shorter, and ironically, the potential reduction involves some of the largest animals on Earth: giant squid.  By sequencing the complete mitochondrial genomes from 43 specimens, Inger Winkelmann and colleagues have shown in the Proceedings of the Royal Society B that there is probably just one species of giant squid, Architeuthis dux.  The finding was a surprise to some, as Architeuthis has had as many as 8 species named (although a morphometric analysis of beaks suggested just one).  I suspect that some of the taxonomic inflation within Architeuthis was a by-product of too few specimens from too few places studied by too many different people (toss in some poor preservation for good measure), perhaps creating an illusion of significant phenotypic gaps. 

In addition to finding no evidence for multiple species, the new study also found very low - bizarrely low - genetic diversity: across the entire mtDNA genome (~20,000 base pairs of DNA) most individuals differ at only ~12 nucleotide positions!  Human mtDNA is well known for lacking diversity, but we typically show 3-7 times more variation (depending on whether it’s African or non-African mtDNA).  The sample sizes from any one place are pretty small, but it’s hard to believe that the sampling failed to find any common but older haplotypes just by chance.  Another totally weird aspect of giant squid mtDNA is a large duplication of several mtDNA genes.  Overall, the patterns of mtDNA variation in giant squid are very unusual, to say the least. 

The data also showed high genetic homogeneity across the entire species' range.  It's tempting to think that high rates of migration of planktonic larvae explains the spatial homogeneity, but, as the authors point out, a rapid range expansion can create the illusion of high contemporary rates of migration.  Gene flow is often the go-to explanation for patterns of high genetic homogeneity in marine species, but it actually takes quite a bit of gene flow to maintain allele frequencies among populations.  Sewall Wright's (1951) famous "one-migrant-per-generation" (OMPG) rule is often invoked as a threshold to maintain equal allele frequencies ("panmixia") among populations, but what Wright was talking about was that OMPG can be enough to prevent the negative fitness effects of inbreeding.  Something more like 10-15 migrants per generation (every generation) is necessary to equalize allele frequencies (Wright, 1969; Waples & Gaggiotti, 2006; Lowe and Allendorf, 2010).  Could that many larvae be exchanged between ocean basins each generation?  Whatever the case, it will be very interesting to see what more data have to say about actual rates of exchange between ocean basins.  Unfortunately, it may take some time to get enough samples to make those estimates.

The fact that we know so little about an abundant organism roughly the length of a school bus only highlights to me how much remains to be learned about the inhabitants of our oceans, especially with respect to basic questions of abundance and diversity, both among and within species.  Sometimes, discovery and description of taxa gets undervalued as science because the work doesn't always start from a specific question or hypothesis, but instead a desire to simply find and catalogue what's out there.  However, as the work by Winklemann and colleagues shows, characterizing patterns of diversity is the fundamental first step towards understanding the processes that generate diversity.

Literature Cited

Lowe, W. H. and F. W. Allendorf. 2010. What can genetics tell us about population connectivity? Molecular Ecology 19: 3038-3051.

Waples R. S. and O. Gaggiotti. 2006. What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology, 15, 1419–1439.

Wright, S. 1951. The genetical structure of natural populations. Annals of Eugenics, 15, 323–354.

Wright, S. 1969. Evolution and the Genetics of Populations, Vol. 2. University of Chicago Press, Chicago, IL.