Phenotypic links among life-history stages are complex and context-dependent in a marine invertebrate: interactions among offspring size, larval nutrition and postmetamorphic density

Authors: Richard M Allen and Dustin J Marshall

Published in: Functional Ecology, volume 27, issue 6 (December 2013)


Examples of simple phenotypic relationships, where variation in one stage directly affects phenotypic variation in a subsequent stage, are documented in most taxa. However, environmental variation can mediate these relationships, and because most organisms develop through multiple life-history stages, each stage-dependent environment has the potential to create new phenotypic relationships and interfere with existing relationships.

Despite the likelihood of complex phenotypic interactions among life-history stages, and the potential for these interactions to resonate throughout the life history, there are few tests of the problem and few predictions of how these phenotypic interactions are resolved.

Hydroides diramphus
Hydroides diramphus, a polychaete tube worm found in cosmopolitan benthic marine assemblages. Image by Richard Allen.

Here, we examined the interdependent effects of three sources of phenotypic variation on the performance of a marine tube worm. Sources of phenotypic variation included: offspring size, larval nutrition and juvenile density.

We found highly context-dependent relationships between these factors and postmetamorphic performance. Within the overarching result of context dependence, we found: interactions could negate and reverse relationships; early-stage phenotypes could persist to postmetamorphosis; later, life-history environments could contribute more to recruit phenotypes than early-stages; and late-stage variation can depend on early-stage phenotypes.

Our results demonstrate that while simple phenotypic links among the egg, larval and post-recruitment stages may be common and important contributors to growth and survival, these relationships should be considered in the context of the organism’s life experience. Each phenotypic link among stages can potentially be complex and depend on prior experience, current state and the subsequent environments experienced.

Full paper

Allen R, Marshall DJ (2013) Phenotypic links among life-history stages are complex and context-dependent in a marine invertebrate: interactions among offspring size, larval nutrition, and post-metamorphic density. Functional Ecology, 27(6): 1358–1366 PDFPDF 390 KB doi: 10.1111/1365-2435.12117

Fertilisation is not a new beginning: sperm environment affects offspring developmental success

Authors: Hannah Ritchie and Dustin J Marshall

Published in: The Journal of Experimental Biology, volume 216 (August 2013)


For organisms with complex life histories, the direction and magnitude of phenotypic links among life-history stages can have important ecological and evolutionary effects.

While the phenotypic links between mothers and offspring, as well as between larvae and adults, are well recognised, the links between sperm phenotype and offspring phenotype have been less well explored.

Here, we used a split-clutch / split-ejaculate design to examine whether the environment that sperm experience affects the subsequent performance of larvae in the broadcast spawning marine invertebrate Galeolaria gemineoa. The environment that sperm experienced affected the developmental success of larvae sired by these sperm; larvae sired by sperm that experienced low salinities had poorer developmental success than larvae sired by sperm that experienced a normal salinity.

When we explored the interactive effects of the sperm environment and the larval environment with an orthogonal design, we found an interaction; when sperm and larvae experienced the same environment, performance was generally higher than when the sperm and larval environments differed. These effects could be due to selection on specific sperm phenotypes, phenotypic modification of the sperm or both.

Together, our results challenge the traditional notion that sperm are merely transporters of genetic material; instead, significant covariance between sperm and offspring phenotypes exists. Our study adds to a growing list that demonstrates that fertilisation does have a homogenising effect on the phenotype of the zygote, and that events before fertilisation during the gamete phase can carry through to affect performance in later life-history stages.

Full paper

Ritchie H, Marshall DJ (2013) Fertilisation is not a new beginning: sperm environment affects offspring developmental success. The Journal of Experimental Biology, 216 (16), 3104–3109  PDFPDF 254 KB doi:10.1242/jeb.087221

The biogeography of marine invertebrate life histories

Authors: Dustin J Marshall, Patrick J Krug, Elena K Kupriyanova, Maria Byrne and Richard B Emlet

Published in: Annual Review of Ecology, Evolution and Systematics, volume 43, pp. 97–114, doi: 10.1146/annurev-ecolsys-102710-145004


Biologists have long sought to identify and explain patterns in the diverse array of marine life histories. The most famous speculation about such patterns is Gunnar Thorson’s suggestion that species producing planktonic larvae are rarer at higher latitudes (Thorson’s rule). Although some elements of Thorson’s rule have proven incorrect, other elements remain untested.

With a wealth of new life-history data, statistical approaches, and remote-sensing technology, new insights into marine reproduction can be generated.

We gathered life-history data for more than 1,000 marine invertebrates and examined patterns in the prevalence of different life histories. Systematic patterns in marine life histories exist at a range of scales, some of which support Thorson, whereas others suggest previously unrecognized relationships between the marine environment and the life histories of marine invertebrates.

Overall, marine life histories covary strongly with temperature and local ocean productivity, and different regions should be managed accordingly.

Full paper

Marshall DJ, Krug PJ, Kupriyanova EK, Byrne M, Emlet RB (2012) The biogeography of marine invertebrate life-histories. Annual Review of Ecology, Evolution and Systematics, 43: 97–114 External linke-print doi: 10.1146/annurev-ecolsys-102710-145004