Thursday, May 2, 2013

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. 2University of Chicago Press, Chicago, IL.

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