Research

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the October cover of
The Biological Bulletin.

Gamete compatibility and

Speciation in Arctic sea urchins

Selective forces that shape the evolution of gamete morphology are complex, and the links between gamete morphology, reproductive isolation and genetic divergence remain elusive. In marine invertebrates, positive selection on reproductive traits is thought to drive the rapid divergence of sperm and egg proteins. Likewise, sexual selection has been implicated in the evolution of egg size and egg accessory coats. A similar role has been suggested for sperm morphology but while basic sperm morphology has been described for many marine invertebrates, few data exist on within species variation in sperm traits, and the underlying genetic architecture remains to be examined. Unraveling the consequences and adaptive significance of within-species variation in sperm morphology and its pattern among free-spawning invertebrates may help elucidate the evolution of reproductive isolation, and thus the mechanisms that underlie the formation of new marine species.

          Together with collaborators, I document among-population variation in 
sperm morphology that is correlated with population divergence in neutral genetic 
markers, and possibly with adaptive features of reproductive compatibility. This is 
an expanding area, especially in echinoderms in which it's possible to assay variation 
in gamete compatibility in vitro and parallel variation at some of the loci that encode 
gamete recognition molecules. Combined with the use of microsatellites for paternity 
analysis (allowing for experimental investigations into, for example, sperm precedence 
among individuals and species), this is a tractable system for enquiries into the genetic 
basis of species recognition, species-specific gamete traits and life-history evolution. 
Comparing adaptive traits within and among species and populations from different 
oceans and  latitudes  – from temperate to high arctic ecosystems, allows for results to 
be interpreted in the context of adaptation to climate change, in addition to testing 
theoretical evolutionary models.

In other work, I empirically test current theory on egg-size evolution and the role of gamete traits and sperm availability. Here, we directly address an ongoing controversy about the effect of egg-accessory coats on fertilization success and egg-size evolution, and thus the evolution of anisogamy.
Strongylocentrotus droebachiensis shows spectacular intraspecific variation in egg size with latitude along the Norwegian coast, and variation in egg jelly-coat thickness that is inversely proportional to egg size. We use this geographic gradient to experimentally test the combined effects of egg and accessory-coat size on fertilization success. We show that the 'egg fertilizability' (the chance that a sperm will fertilize an egg if it encounters one) varies with target size and sperm concentration, and thus that the sea urchin system violates an assumption of the most widely used model of fertilization kinetics. We suggest the need to incorporate into existing fertilization kinetics models the interactions between egg size, total target size, and accessory-coat thickness, and how these vary with sperm concentration.

In free-spawning organisms, the risk of both incomplete fertilization (related to sperm limitation) and lethal fertilization by more than one sperm (under conditions of sperm competition) may influence the evolution of traits related to fertilization success. Given increasing evidence for great environmental heterogeneity in sperm concentration during natural spawning events, we provide evidence that studies of fertilization dynamics in free-spawning organisms should consider the role of egg-accessory coats in terms of a possible tradeoff between egg size and total target size and its complicated relationship to sperm.

Publications

Marks, J.A., Biermann, C.H., Earnes, W.F. and H. Kryvi. 2008. Sperm polymorphism within the sea urchin strongylocentrotus droebachiensis: Divergence between Pacific and Atlantic oceans. Biol. Bull. 215: 115-125. pdf

Biermann, C. H., Marks, J. A., Vilela-Silva, A-C. E. S.- Castro, M. O. and P. A. S. Mourão. 2004. Carbohydrate-based species recognition in sea urchin fertilization: another avenue for speciation? Evolution and Development 6(5): 353-361. pdf

Biermann, C. H. and J. A. Marks. 2000. Geographic divergence of gamete recognition systems in two species of the sea urchin genus Strongylocentrotus. Zygote 8 (S):86-87. pdf

Marks, J.A., Biermann, C.H., Heegaard, E. and A. Breistøl. (submitted ms.). Sperm availability and the evolution of egg and jelly-coat size in a free-spawning marine invertebrate.

Marks, J. A. and Aarset, B. 2004. Kråkeboller – fra pest til gullgruve? Norsk Fiskeoppdrett 29(4):32-34. pdf

Collaborators: C. Biermann, E. Heegaard, A. Breistøl.

Population genetics

Photo: C. Biermann

Photo: C. Biermann
Understanding marine population connectivity is critical for sustainable management of marine resources. The degree to which populations of marine organisms exchange migrants determines whether they function as one large metapopulation or many independent units and thus influences their response to potential disturbance from harvesting, habitat destruction or climate change. As such, knowledge of connectivity directly impacts management decisions and addresses the question of whether fisheries management and the design of marine protected areas should be tailored to variation in coastal geography and regional oceanographic conditions.

It is often assumed that marine species with long-lived planktonic larvae disperse great distances in ocean currents and will thus exhibit low levels of genetic differentiation. However, recent evidence shows that significant population-genetic subdivision may occur even in species with a long larval duration and that variability in ocean currents can influence the spatial genetic structure of marine populations.

We are presently working to determine the population genetic structure of the sea urchins Strongylocentrotus droebachiensis and Strongylocentrotus pallidus along the Norwegian coast and Svalbard, using a fragment of the cytochrome c oxidase I gene (COI) of the mitochondrion and microsatellite assays. Is there genetic differentiation of separate populations, or clinal variation within genetically continuous populations? How do these populations compare to samples from Greenland, the eastern Pacific and western Atlantic oceans?

The common green sea urchin, Strongylocentrotus droebachiensis has a circumarctic distribution, and shows substantial genetic subdivision between northeastern Atlantic populations and northwestern Atlantic and Pacific populations (Marks et al. 2004). Norwegian populations show significant divergence from their Pacific counterparts in both mitochondrial DNA (Addison and Hart, 2005) and nuclear DNA (sperm bindin: Marks et al. 2008; microsatellites: Addison and Hart, 2004; 2005). Little is known, however, about fine-scale populations subdivisions within these regions. The high degree of genetic divergence among S. droebachiensis populations (> 1.5% in bindin; 3.5% in mtDNA) is in fact greater than that separating several species pairs of Indo-West Pacific sea urchins (0.9%; Landry et al., 2003). Northwestern Atlantic S. droebachiensis populations contain a mixture of alleles from both northern Pacific and European sources (Addison and Hart, 2004; 2005; Harper et al., 2007; Palumbi and Wilson, 1990). Fine-scale genetic sampling of S. droebachiensis from the Arctic and northwest Atlantic will shed light on how populations of this species have evolved.

Throughout their geographic range, these urchins exhibit differences in life-history traits including egg size, larval duration and size at metamorphosis (Biermann et al. 2004; Marks, unpublished data). Egg size increases 4-fold in volume along a latitudinal gradient from Sweden to Spitzbergen. Likewise, sperm morphology differs markedly among populations of S. droebachiensis from different oceans, and reflects patterns of genetic divergence (Marks et al. 2008), yet the underlying genetic architecture of these traits remains enigmatic. There is also marked variation in the strength of reproductive barriers (fertilization success) between populations and oceans (Marks and Biermann, unpublished data) and between S. droebachiensis and S. pallidus from different populations (Biermann and Marks 2000).

In many marine fish, both adults and larvae contribute to migration among populations. Sea urchins have benthic adults with relatively little mobility, and population genetic structure will be determined by the interaction of regional oceanographic conditions and life-history traits. As such, the sea urchin system provides a proxy for dispersal of other commercially important organisms with pelagic larvae along the Norwegian coast and Svalbard. This study contributes knowledge of sea urchin population structure that is critical in managing natural populations of urchins and kelp forests and prerequisite for a sustainable commercial urchin fishery developing in Norway today.

Publications

Collaborators: G. Dahle, C. Schander

Didemnid ascidians

Photo: http://woodshole.er.usgs.gov/project-pages/stellwagen/didemnum/

Link to the WHOI marine nuisance species pages for more news on the invasive didemnid sea squirt.

Publications

Marks, J.A. 1993. Systematics and ecology of three didemnid ascidians: Didemnum albidum (Verrill, 1871), Didemnum polare (Hartmeyer, 1903) and Didemnum romssae, new species. Cand.scient. thesis, University of Tromsø, Norway, pp. 89.

Marks, J.A., 1996. Three sibling species of subarctic didemnid ascidians: Didemum albidum (Verrill, 1871), Didemnum polare (Hartmeyer, 1903) and Didemnum romssae, new species. Can. J. Zool. 74:357-379. pdf

Marks, J.A. (unpublished ms.). Contrasting overwintering in two sibling species of arctic marine invertebrate.

Marks, J.A. (ms. in prep. for FishfarmingXpert magazine). Alien sea quirt Didemnum vexillum: invasive tunicate species threatens fish-farming industry.

Other Publications

Padilla, D.K., Harvell, C.D., Marks, J.A. and B. Helmuth. 1996. Induceible aggression and intraspecific competition for space in a marine bryozoan, Membranipora membranecea. Limnol. Oceanog. 41(3):505-512.

Vermeij, G.J., R. B. Lowell, L. J. Walters and J. A. Marks. 1987. Good hosts and their guests: Relations between trochid gastropods and the epizoic limpet Crepidula adunca. The Nautilus. 101(2):69-74.