Shank Lab Journal Club

Shank Laboratory of Molecular Ecology and Evolution, Woods Hole Oceanographic Institution

Resolving postglacial phylogeography using high-throughput sequencing

Authors: Kevin J. EmersonClayton R. Merz, Julian M. Catchen, Paul A. Hohenlohe,William A. Cresko, William E. Bradshaw, and Christina M. Holzapfel

Abstract: The distinction between model and nonmodel organisms is becoming increasingly blurred. High-throughput, second-generation sequencing approaches are being applied to organisms based on their interesting ecological, physiological, developmental, or evolutionary properties and not on the depth of genetic information available for them. Here, we illustrate this point using a low-cost, efficient technique to determine the fine-scale phylogenetic relationships among recently diverged populations in a species. This application of restriction site-associated DNA tags (RAD tags) reveals previously unresolved genetic structure and direction of evolution in the pitcher plant mosquito, Wyeomyia smithii, from a southern Appalachian Mountain refugium following recession of the Laurentide Ice Sheet at 22,000–19,000 B.P. The RAD tag method can be used to identify detailed patterns of phylogeography in any organism regardless of existing genomic data, and, more broadly, to identify incipient speciation and genome-wide variation in natural populations in general.

2. Chromosome-scale selective sweeps shapeCaenorhabditis elegans genomic diversity

Authors: Erik C Andersen, Justin P Gerke, Joshua A Shapiro, Jonathan R Crissman, Rajarshi Ghosh, Joshua S Bloom, Marie-Anne Félix & Leonid Kruglyak

Abstract: The nematode Caenorhabditis elegans is central to research in molecular, cell and developmental biology, but nearly all of this research has been conducted on a single strain of C. elegans. Little is known about the population genomic and evolutionary history of this species. We characterized C. elegans genetic variation using high-throughput selective sequencing of a worldwide collection of 200 wild strains and identified 41,188 SNPs. Notably, C. elegans genome variation is dominated by a set of commonly shared haplotypes on four of its six chromosomes, each spanning many megabases. Population genetic modeling showed that this pattern was generated by chromosome-scale selective sweeps that have reduced variation worldwide; at least one of these sweeps probably occurred in the last few hundred years. These sweeps, which we hypothesize to be a result of human activity, have drastically reshaped the global C. elegans population in the recent past.

Presented by S. Herrera on 15 Feb 2012


Population Genomics of Parallel Adaptation in Threespine Stickleback using Sequenced RAD Tags

Authors: Paul A. Hohenlohe, Susan Bassham, Paul D. Etter,Nicholas Stiffler, Eric A. Johnson, William A. Cresko

Abstract: Next-generation sequencing technology provides novel opportunities for gathering genome-scale sequence data in natural populations, laying the empirical foundation for the evolving field of population genomics. Here we conducted a genome scan of nucleotide diversity and differentiation in natural populations of threespine stickleback (Gasterosteus aculeatus). We used Illumina-sequenced RAD tags to identify and type over 45,000 single nucleotide polymorphisms (SNPs) in each of 100 individuals from two oceanic and three freshwater populations. Overall estimates of genetic diversity and differentiation among populations confirm the biogeographic hypothesis that large panmictic oceanic populations have repeatedly given rise to phenotypically divergent freshwater populations. Genomic regions exhibiting signatures of both balancing and divergent selection were remarkably consistent across multiple, independently derived populations, indicating that replicate parallel phenotypic evolution in stickleback may be occurring through extensive, parallel genetic evolution at a genome-wide scale. Some of these genomic regions co-localize with previously identified QTL for stickleback phenotypic variation identified using laboratory mapping crosses. In addition, we have identified several novel regions showing parallel differentiation across independent populations. Annotation of these regions revealed numerous genes that are candidates for stickleback phenotypic evolution and will form the basis of future genetic analyses in this and other organisms. This study represents the first high-density SNP–based genome scan of genetic diversity and differentiation for populations of threespine stickleback in the wild. These data illustrate the complementary nature of laboratory crosses and population genomic scans by confirming the adaptive significance of previously identified genomic regions, elucidating the particular evolutionary and demographic history of such regions in natural populations, and identifying new genomic regions and candidate genes of evolutionary significance.

Background reading

Presented by S. Herrera on Fri Jan 3rd 2012

‘Hydrogen is an energy source for hydrothermal vent symbioses’


Authors: Jillian M. Petersen,Frank U. Zielinski,Thomas Pape, Richard Seifert, Cristina Moraru,Rudolf Amann, Stephane Hourdez,Peter R. Girguis,Scott D. Wankel,Valerie Barbe,Eric Pelletier, Dennis Fink, Christian Borowski,Wolfgang Bach & Nicole Dubilier

Abstract: The discovery of deep-sea hydrothermal vents in 1977 revolutionized our understanding of the energy sources that fuel primary productivity on Earth. Hydrothermal vent ecosystems are dominated by animals that live in symbiosis with chemosynthetic bacteria. So far, only two energy sources have been shown to power chemosynthetic symbioses: reduced sulphur compounds and methane. Using metagenome sequencing, single-gene fluorescence in situ hybridization, immunohistochemistry, shipboard incubations and in situ mass spectrometry, we show here that the symbionts of the hydrothermal vent mussel Bathymodiolus from the Mid-Atlantic Ridge use hydrogen to power primary production. In addition, we show that the symbionts of Bathymodiolus mussels from Pacific vents have hupL, the key gene for hydrogen oxidation. Furthermore, the symbionts of other vent animals such as the tubeworm Riftia pachyptila and the shrimp Rimicaris exoculataalso have hupL. We propose that the ability to use hydrogen as an energy source is widespread in hydrothermal vent symbioses, particularly at sites where hydrogen is abundant.

Presented by Taylor Heyl on 2011/09/07

‘Caterpillars evolved from onychophorans by hybridogenesis’

PNAS (2009): 0908357106v1-pnas.0908357106


Author: Donald I. Williamson

Abstract: I reject the Darwinian assumption that larvae and their adults evolved from a single common ancestor. Rather I posit that, in animals that metamorphose, the basic types of larvae originated as adults of different lineages, i.e., larvae were transferred when, through hybridization, their genomes were acquired by distantly related animals. “Caterpillars,” the name for eruciforms with thoracic and abdominal legs, are larvae of lepidopterans, hymenopterans, and mecopterans (scorpionflies). Grubs and maggots, including the larvae of beetles, bees, and flies, evolved from caterpillars by loss of legs. Caterpillar larval organs are dismantled and reconstructed in the pupal phase. Such indirect developmental patterns (metamorphoses) did not originate solely by accumulation of random mutations followed by natural selection; rather they are fully consistent with my concept of evolution by hybridogenesis. Members of the phylum Onychophora (velvet worms) are proposed as the evolutionary source of caterpillars and their grub or maggot descendants. I present a molecular biological research proposal to test my thesis. By my hypothesis 2 recognizable sets of genes are detectable in the genomes of all insects with caterpillar grub- or maggot-like larvae: (i) onychophoran genes that code for proteins determining larval morphology/physiology and (ii) sequentially expressed insect genes that code for adult proteins. The genomes of insects and other animals that, by contrast, entirely lack larvae comprise recognizable sets of genes from single animal common ancestors.

Also to be discussed, responses to this paper:

Presented by Santiago Herrera and Catriona Munro on 2011/09/02

‘Phylogeography of a pan-Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic’

Molecular Ecology (2011) 20 (4):829–843

doi: 10.1111/j.1365-294X.2010.04978.x

Authors: ETTER, R. J., BOYLE, E. E., GLAZIER, A., JENNINGS, R. M., DUTRA, E. and CHASE, M. R.

Abstract: The deep sea is a vast and essentially continuous environment with few obvious barriers to gene flow. How populations diverge and new species form in this remote ecosystem is poorly understood. Phylogeographical analyses have begun to provide some insight into evolutionary processes at bathyal depths (<3000 m), but much less is known about evolution in the more extensive abyssal regions (>3000 m). Here, we quantify geographical and bathymetric patterns of genetic variation (16S rRNA mitochondrial gene) in the protobranch bivalve Ledella ultima, which is one of the most abundant abyssal protobranchs in the Atlantic with a broad bathymetric and geographical distribution. We found virtually no genetic divergence within basins and only modest divergence among eight Atlantic basins. Levels of population divergence among basins were related to geographical distance and were greater in the South Atlantic than in the North Atlantic. Ocean-wide patterns of genetic variation indicate basin-wide divergence that exceeds what others have found for abyssal organisms, but considerably less than bathyal protobranchs across similar geographical scales. Populations on either side of the Mid-Atlantic Ridge in the North Atlantic differed, suggesting the Ridge might impede gene flow at abyssal depths. Our results indicate that abyssal populations might be quite large (cosmopolitan), exhibit only modest genetic structure and probably provide little potential for the formation of new species.

Presented by Annette Govindarajan on 2011/9/24

‘Survival of mussels in extremely acidic waters on a submarine volcano’

Nature Geoscience (2009) 2, 344 – 348


Authors: Verena Tunnicliffe, Kimberley T. A. Davies, David A. Butterfield, Robert W. Embley, Jonathan M. Rose & William W. Chadwick Jr


Increasing atmospheric carbon dioxide levels are causing ocean acidification, compromising the ability of some marine organisms to build and maintain support structures as the equilibrium state of inorganic carbon moves away from calcium carbonate. Few marine organisms tolerate conditions where ocean pH falls significantly below today’s value of about 8.1 and aragonite and calcite saturation values below 1. Here we report dense clusters of the vent musselBathymodiolus brevior in natural conditions of pH values between 5.36 and 7.29 on northwest Eifuku volcano, Mariana arc, where liquid carbon dioxide and hydrogen sulphide emerge in a hydrothermal setting. We find that both shell thickness and daily growth increments in shells from northwest Eifuku are only about half those recorded from mussels living in water with pH>7.8. Low pH may therefore also be implicated in metabolic impairment. We identify four-decade-old mussels, but suggest that the mussels can survive for so long only if their protective shell covering remains intact: crabs that could expose the underlying calcium carbonate to dissolution are absent from this setting. The mussels’ ability to precipitate shells in such low-pH conditions is remarkable. Nevertheless, the vulnerability of molluscs to predators is likely to increase in a future ocean with low pH.

Presented by Catriona Munro on 2011/8/17

‘Genetic diversity and connectivity of deep-sea hydrothermal vent metapopulations’

Molecular Ecology (2010) 19(20):4391-4411

doi: 10.1111/j.1365-294X.2010.04789.x

Author: Robert C. Vrijenhoek


Deep-sea hydrothermal vents provide ephemeral habitats for animal communities that depend on chemosynthetic primary production. Sporadic volcanic and tectonic events destroy local vent fields and create new ones. Ongoing dispersal and cycles of extirpation and colonization affect the levels and distribution of genetic diversity in vent metapopulations. Several species exhibit evidence for stepping-stone dispersal along relatively linear, oceanic, ridge axes. Other species exhibit very high rates of gene flow, although natural barriers associated with variation in depth, deep-ocean currents, and lateral offsets of ridge axes often subdivide populations. Various degrees of impedance to dispersal across such boundaries are products of species-specific life histories and behaviours. Though unrelated to the size of a species range, levels of genetic diversity appear to correspond with the number of active vent localities that a species occupies within its range. Pioneer species that rapidly colonize nascent vents tend to be less subdivided and more diverse genetically than species that are slow to establish colonies at vents. Understanding the diversity and connectivity of vent metapopulations provides essential information for designing deep-sea preserves in regions that are under consideration for submarine mining of precious metals.

Presented by Catriona Munro on 2011/8/3

‘Beyond DNA: integrating inclusive inheritance into an extended theory of evolution’

Nature Reviews Genetics (2011) 12, 475-486


Authors: Étienne Danchin, Anne Charmantier, Frances A. Champagne, Alex Mesoudi, Benoit Pujol & Simon Blanchet


Many biologists are calling for an ‘extended evolutionary synthesis’ that would ‘modernize the modern synthesis’ of evolution. Biological information is typically considered as being transmitted across generations by the DNA sequence alone, but accumulating evidence indicates that both genetic and non-genetic inheritance, and the interactions between them, have important effects on evolutionary outcomes. We review the evidence for such effects of epigenetic, ecological and cultural inheritance and parental effects, and outline methods that quantify the relative contributions of genetic and non-genetic heritability to the transmission of phenotypic variation across generations. These issues have implications for diverse areas, from the question of missing heritability in human complex-trait genetics to the basis of major evolutionary transitions.

Presented by Santiago Herrera on 2011/7/27