Revealing hidden evolutionary capacity to cope with global change

Authors: Evatt Chirgwin, Keyne Monro, Carla M Sgró And Dustin J Marshall

Published in: Global Change Biology, volume 21, issue 9 (September 2015)


The extent to which global change will impact the long-term persistence of species depends on their evolutionary potential to adapt to future conditions.

While the number of studies that estimate the standing levels of adaptive genetic variation in populations under predicted global change scenarios is growing all the time, few studies have considered multiple environments simultaneously and even fewer have considered evolutionary potential in multi- variate context.

Because conditions will not be constant, adaptation to climate change is fundamentally a multivariate process so viewing genetic variances and covariances over multivariate space will always be more informative than relying on bivariate genetic correlations between traits. A multivariate approach to understanding the evolutionary capacity to cope with global change is necessary to avoid misestimating adaptive genetic variation in the dimensions in which selection will act.

We assessed the evolutionary capacity of the larval stage of the marine polychaete Galeolaria caespitosa to adapt to warmer water temperatures. Galeolaria is an important habitat-forming species in Australia, and its earlier life-history stages tend to be more susceptible to stress. We used a powerful quantitative genetics design that assessed the impacts of three temperatures on subsequent survival across over 30,000 embryos across 204 unique families.

We found adaptive genetic variation in the two cooler temperatures in our study, but none in the warmest temperature. Based on these results, we would have concluded that this species has very little capacity to evolve to the warmest temperature. However, when we explored genetic variation in multivariate space, we found evidence that larval survival has the potential to evolve even in the warmest temperatures via correlated responses to selection across thermal environments.

Future studies should take a multivariate approach to estimating evolutionary capacity to cope with global change lest they misestimate a species’ true adaptive potential.


Chirgwin E, Monro K, Sgró CM, Marshall DJ (2015) Revealing hidden evolutionary capacity to cope with global change. Global Change Biology, 21: 3356–3366. PDF 230 KB doi: 10.1111/gcb.12929


Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space

Authors: J Robin Svensson and Dustin J Marshall

Published in: Ecology, volume 96, issue 3 (March 2015)


Much of our understanding of competition comes from observations in sessile systems, such as rainforests and marine invertebrate communities.

In terrestrial systems, sessile species often compete for multiple limiting resources (i.e., space, light, and nutrients), but in marine systems, space is viewed as the primary or sole limiting resource. Competition theory, on the other hand, suggests that competition for a single limiting resource is unlikely to maintain high species diversity, but manipulative tests of competition for other resources in marine benthic systems are exceedingly rare.

Here, we manipulate the availability of food for a classic system, marine sessile invertebrate communities, and investigate the effects on species diversity, abundance, and composition during early succession as well as on the growth of bryozoan populations in the field.

We found the number of species to be greater, available space to be lower, and the community composition to be different in assemblages subjected to increased food availability compared to controls. Similarly, laboratory-settled bryozoans deployed into the field grew more in the presence of enhanced food.

Our results suggest that food can act as a limiting resource, affecting both diversity and abundance, even when bare space is still available in hard-substratum communities. Consequently, broadening the view of resource limitation beyond solely space may increase our understanding and predictability of marine sessile systems.


Svensson R, Marshall DJ (2015) Limiting resources in sessile systems: food enhances diversity and growth of suspension feeders despite available space, Ecology, 96(3) 819–827 PDF 836 KB doi:10.1890/14-0665.1

Non-contact competition in a sessile marine invertebrate: causes and consequences

Authors: Matthew L Thompson, Dustin J Marshall and Keyne Monro

Published in: Marine Ecology Progress Series, volume 522 (March 2015)


In marine benthic communities, phenotypic responses to contact competition are
well resolved, but the causes and consequences of non-contact competition remain unclear.

Here, we used the arborescent bryozoan Bugula neritina to firstly identify whether colonies change their phenotype as a result of non-contact competition, and then understand the mechanism behind the changes. Secondly, we determined the phenotypes that change in response to non-contact competition, with focus on changes in the feeding structure, viz. the lophophore. Lastly, we used a reciprocal transplant design to test whether phenotypic responses to non-contact competition reduce its negative effects.

We found that phenotypic responses to non-contact competition were mediated by the biological effects of conspecific neighbours, but were also determined by the physical effects associated with increased density. Further, we found that colonies grown in high
conspecific density environments were smaller (though more elongated for their size) and had smaller lophophores than colonies from low conspecific density treatments. However, we found no evidence that such phenotypic responses constituted adaptive plasticity; instead, individuals that experienced non-contact competition always performed worse than individuals that had not, and the effects of exposure to non-contact competition were additive.

Our study suggests that noncontact competition is an important and persistent process in benthic marine communities, but that phenotypic plasticity, though present, does not buffer individuals from the negative effects of this process.


Thompson ML, Marshall DJ, Monro K (2015) Non-contact competition in a sessile marine invertebrate: causes and consequences. Marine Ecology Progress Series, 522:115–125 doi: 10.3354/meps11178

Deconstructing environmental predictability: seasonality, environmental colour and the biogeography of marine life histories

Authors: Dustin J Marshall and Scott C Burgess

Published in: Ecology Letters, volume 18, issue 2 (February 2015)


Environmental predictability is predicted to shape the evolution of life histories. Two key types of environmental predictability, seasonality and environmental colour, may influence life-history evolution independently but formal considerations of both and how they relate to life history are exceedingly rare.

Here, in a global biogeographical analysis of over 800 marine invertebrates, we explore the relationships between both forms of environmental predictability and three fundamental life-history traits: location of larval development (aplanktonic vs. planktonic), larval develop- mental mode (feeding vs. non-feeding) and offspring size.

We found that both dispersal potential and offspring size related to environmental predictability, but the relationships depended on both the environmental factor as well as the type of predictability. Environments that were more seasonal in food availability had a higher prevalence of species with a planktonic larval stage.

Future studies should consider both types of environmental predictability as each can strongly affect life-history evolution.


Marshall DJ, Burgess SC (2015) Deconstructing environmental predictability: seasonality, environmental color and the biogeography of marine life histories, Ecology Letters, 18, 174–181 PDF 1.2 MB doi:10.1111/ele.12402

Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

Author: Dustin J Marshall

Published in: The Journal of Experimental Biology, volume 208, issue 1 (January 2015)


Traditionally, it has been assumed that sperm are a vehicle for genes and nothing more. As such, the only source of variance in offspring phenotype via the paternal line has been genetic effects. More recently, however, it has been shown that the phenotype or environment of fathers can affect the phenotype of offspring, challenging traditional theory with implications for evolution, ecology and human in vitro fertilisation.

Here, I review sources of non-genetic variation in the sperm phenotype and evidence for co-variation between sperm and offspring phenotypes. I distinguish between two environmental sources of variation in sperm phenotype: the pre- release environment and the post-release environment.

Pre-release, sperm phenotypes can vary within species according to male phenotype (e.g. body size) and according to local conditions such as the threat of sperm competition. Post-release, the physicochemical conditions that sperm experience, either when freely spawned or when released into the female reproductive tract, can further filter or modify sperm phenotypes.

I find evidence that both pre- and post-release sperm environments can affect offspring phenotype; fertilisation is not a new beginning – rather, the experiences of sperm with the father and upon release can drive variation in the phenotype of the offspring.

Interestingly, there was some evidence for co-variation between the stress resistance of sperm and the stress resistance of offspring, though more studies are needed to determine whether such effects are widespread.

Overall, it appears that environmentally induced covariation between sperm and offspring phenotypes is non-negligible and further work is needed to determine their prevalence and strength.


Marsall DJ (2015) Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects, The Journal of Experimental Biology, 208(1), 107–113 PDF 458 KB doi:10.1242/jeb.106427

Larval size and age affect colonization in a marine invertebrate

Authors: Dustin J Marshall and Peter D Steinberg

Published in: The Journal of Experimental Biology, volume 217, issue 22 (November 2014)


The relationship between offspring size and performance determines the optimal trade-off between producing many small offspring or fewer large offspring and the existence of this relationship has become a central tenet of life-history theory.

For organisms with multiple life-history stages, the relationship between offspring size and performance is the product of the effects of offspring size in each life-history stage.

Marine invertebrates have long been a model system for examining the evolutionary ecology of offspring size, and whilst offspring size effects have been found in several life-history stages, the crucial stage of colonization has received less attention.

We examined the effect of offspring size on the settlement response of sea-urchin larvae (Heliocidaris erythrogramma) to preferred and less preferred hostplants, how these effects changed over the larval period and estimated the success of juveniles in the field on preferred and less preferred host plants.

We found that smaller larvae became competent to respond to preferred host plant cues sooner than larger larvae but larger larvae rejected less preferred host plants for longer than smaller larvae. Overall, smaller H. erythrogramma larvae are likely to have less dispersal potential and are more likely to settle in less preferred habitats whereas larger larvae appear to have an obligately longer dispersal period but settle in preferred habitats.

Our results suggest that marine invertebrates that produce non-feeding larvae may have the potential to affect the dispersal of their offspring in previously unanticipated ways and that offspring size is subject to a complex web of selection across life-history stages.


Marshall DJ, Steinberg PD (2014) Larval size and age affect colonization in a marine invertebrate, Journal of Experimental Biology, 217: 3981–3987 PDF 403 KB doi:10.1242/jeb.111781

Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus

Authors: Richard M Allen and Dustin J Marshall

Published in: PloS ONE, volume 9, issue 7 (July 2014)


The optimal balance of reproductive effort between offspring size and number depends on the fitness of offspring size in a particular environment.

The variable environments offspring experience, both among and within life-history stages, are likely to alter the offspring size/fitness relationship and favor different offspring sizes. Hence, the many environments experienced throughout complex life-histories present mothers with a significant challenge to optimally allocate their reproductive effort.

In a marine annelid, we tested the relationship between egg size and performance across multiple life-history stages, including: fertilization, larval development, and post-metamorphosis survival and size in the field.

We found evidence of conflicting effects of egg size on performance: larger eggs had higher fertilization under sperm-limited conditions, were slightly faster to develop pre-feeding, and were larger post-metamorphosis; however, smaller eggs had higher fertilization when sperm was abundant, and faster planktonic development; and egg size did not affect post-metamorphic survival.

The results indicate that egg size effects are conflicting in H. diramphus depending on the environments within and among life-history stages. We suggest that offspring size in this species may be a compromise between the overall costs and benefits of egg sizes in each stage and that performance in any one stage is not maximized.


Allen RM, Marshall DJ (2014) Egg size effects across multiple life-history stages in the marine annelid Hydroides diramphus. PLoS ONE 9(7): e102253 PDF 250 KB doi:10.1371/journal.pone.0102253

Local gamete competition explains sex allocation and fertilization strategies in the sea

Authors: Jonathan M Henshaw, Dustin J Marshall, Michael D Jennions and Hanna Kokko

Published in: The American Naturalist, volume 184, number 2 (August 2014)


Within and across taxa, there is much variation in the mode of fertilization, that is, whether eggs and/or sperm are released or kept inside or on the surface of the parent’s body.

Although the evolutionary consequences of fertilization mode are far reaching, transitions in the fertilization mode itself have largely escaped theoretical attention.

Here we develop the first evolutionary model of egg retention and release, which also considers transitions between hermaphroditism and dioecy as well as egg size evolution. We provide a unifying explanation for reported associations between small body size, hermaphroditism, and egg retention in marine invertebrates that have puzzled researchers for more than three decades.

Our model, by including sperm limitation, shows that all these patterns can arise as an evolutionary response to local competition between eggs for fertilization. This can provide a general explanation for three empirical patterns:

  • sperm casters tend to be smaller than related broadcast spawners,
  • hermaphroditism is disproportionately common in sperm casters, and
  • offspring of sperm casters are larger.

Local gamete competition also explains a universal sexual asymmetry: females of some species retain their gametes while males release theirs, but the opposite (“egg casting”) lacks evolutionary stability and is apparently not found in nature.


Henshaw JM, Marshall DJ, Jennions MD, Kokko H (2014) Local gamete competition explains sex allocation and fertilization strategies in the sea. The American Naturalist, 184 E32–E49 PDF 737 KB DOI: 10.1086/676641

Supplementary information: Data for robustness analysis XLSX 1 MB

Relative influence of resident species and environmental variation on community assembly

Authors: Arthur Riedel, Keyne Monro, Mark W Blows and Dustin J Marshall

Published in: Marine Ecology Progress Series, volume 499 (March 2014)


Prior residence by a species can affect subsequent community assembly. However, previous studies insulated their focal communities from additional sources of variation, and the role of resident species in the context of environmental heterogeneity is rarely considered.

If environmental and resident species effects act independently, then each should be broadly predictable, and their contribution to community assembly should be quantifiable in relation to each other. Alternatively, if effects interact, their combination may explain more of the differences in communities than the additive influence of each alone.

We estimated the effects of a common, early-colonising resident (the encrusting bryozoan Hippopodina iririkiensis) on community assembly relative to substrate orientation. Some species showed complex responses in association with orientation, with positive responses in one orientation, negative in the other. Variation in orientation explained the majority of variation in overall community assembly. Variation among the panels holding replicates of our resident species, a blocking factor in the analysis, permitted us to consider small-scale spatial variation.

Abundances responded to resident species effects but interacted with spatial variation: the impact of the resident species on community assembly varied with orientation and space. Functional groups showed similarly idiosyncratic responses to the prior resident.

Overall, we found that resident species effects were weak relative to the effects of environmental variation on community assembly. Furthermore, those resident species effects that we did detect were inconsistent across environments, suggesting that this species has little predictable influence on community assembly.

Environmental variation may be an important contributor and requires more widespread consideration to better understand how resident species effects act in nature.


Riedel A, Monro K, Blows MW, Marshall DJ (2014) Relative influence of resident species and environmental variation on community assembly. Marine Ecology Progress Series 499: 103–113 PDF 448 KB DOI:10.3354/meps10695

The genetic covariance between life cycle stages separated by metamorphosis

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

Published in: Proceedings of the Royal Society B, volume 281 number 1788 (July 2014)


Metamorphosis is common in animals, yet the genetic associations between life cycle stages are poorly understood.

Given the radical changes that occur at metamorphosis, selection may differ before and after metamorphosis, and the extent that genetic associations between pre- and post-metamorphic traits constrain evolutionary change is a subject of considerable interest. In some instances, metamorphosis may allow the genetic decoupling of life cycle stages, whereas in others, metamorphosis could allow complementary responses to selection across the life cycle.

Using a diallel breeding design, we measured viability at four ontogenetic stages (embryo, larval, juvenile and adult viability), in the ascidian Ciona intestinalis and examined the orientation of additive genetic variation with respect to the metamorphic boundary.

We found support for one eigenvector of G (gobsmax), which contrasted larval viability against embryo viability and juvenile viability. Target matrix rotation confirmed that while gobsmax shows genetic associations can extend beyond metamorphosis, there is still considerable scope for decoupled phenotypic evolution.

Therefore, although genetic associations across metamorphosis could limit that range of phenotypes that are attainable, traits on either side of the metamorphic boundary are capable of some independent evolutionary change in response to the divergent conditions encountered during each life cycle stage.

Full paper

Aguirre JD, Blows MW, Marshall DJ (2014) The genetic covariance between life cycle stages separated by metamorphosis. Proceedings of the Royal Society B. 281: 20141091. PDF 554 KB DOI 10.1098/rspb.2014.1091