Genetic compatibility underlies benefits of mate choice in an external fertilizer

Authors: J David Aguirre, Mark W Blows, and Dustin J Marshall

Published in: The American Naturalist, volume 187, number 5 (May 2016)


Mate choice is a common feature of sexually reproducing species. In sessile or sedentary external fertilizers, however, direct interactions between reproductive partners are minimal, and instead mate recognition and choice must occur at the level of gametes.

It is common for some sperm and egg combinations to have higher fertilization success than others, but it remains unclear whether differences in fertilization reflect gamete-level mate choice (GMC) for paternal quality or parental compatibility.

Here, we examine the mechanisms underlying GMC in an externally fertilizing ascidian. A manipulative mate-choice assay confirmed that offspring viability was greater in clutches where we allowed GMC than in clutches where we precluded GMC. A complementary quantitative genetic experiment then revealed that paternal quality effects were generally weaker than parental compatibility effects, particularly for the trait combination underlying the benefits of GMC.

Overall, our data suggest that gametes that are more compatible at fertilization produce more viable offspring than gametes that are less compatible at fertilization. Therefore, although the regalia we typically associate with sexual selection are absent in external fertilizers, mechanisms that allow females to bias fertilization in favor of some males over others produce significant fitness benefits in organisms reproducing via the ancestral strategy.


Aguirre, JD, Blows MW, Marshall DJ (2016) Genetic compatibility underlies benefits of mate choice in an external fertiliser. The American Naturalist, 187(5) DOI: 10.1086/685892 PDF 672 KB

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

Genetic diversity increases population productivity in a sessile marine invertebrate

Authors: J David Aguirre and Dustin J Marshall

Published in: Ecology, volume 93, issue 5, doi: 10.1890/11-1448.1


Reductions in genetic diversity can have widespread ecological consequences: populations with higher genetic diversity are more stable, productive and resistant to disturbance or disease than populations with lower genetic diversity.

These ecological effects of genetic diversity differ from the more familiar evolutionary consequences of depleting genetic diversity, because ecological effects manifest within a single generation.

If common, genetic diversity effects have the potential to change the way we view and manage populations, but our understanding of these effects is far from complete, and the role of genetic diversity in sexually reproducing animals remains unclear.

Here, we examined the effects of genetic diversity in a sexually reproducing marine invertebrate in the field. We manipulated the genetic diversity of experimental populations and then measured individual survival, growth, and fecundity, as well as the size of offspring produced by individuals in high and low genetic diversity populations.

Overall, we found greater genetic diversity increased performance across all metrics, and that complementarity effects drove the increased productivity of our high-diversity populations.

Our results show that differences in genetic diversity among populations can have pervasive effects on population productivity within remarkably short periods of time.

Full paper

Aguirre JD, Marshall DJ (2012) Genetic diversity increases population productivity in a sessile marine invertebrate. Ecology 93: 1134–1142 PDFPDF 1.3 MB doi: 10.1890/11-1448.1