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 diramphus 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

Adaptive parental effects: the importance of estimating environmental predictability and offspring fitness appropriately

Authors: Scott C Burgess and Dustin J Marshall

Published in: Oikos, volume 123, issue 7 (July 2014)


Anticipatory parental effects (APEs) occur when parents adjust the phenotype of their offspring to match the local environment, so as to increase the fitness of both parents and offspring.

APEs, as in the evolution of adaptive phenotypic plasticity more generally, are predicated on the idea that the parental environment is a reliable predictor of the offspring environment.

Most studies on APEs fail to explicitly consider environmental predictability so risk searching for APEs under circumstances where they are unlikely to occur. This failure is perhaps one of the major reasons for mixed evidence for APEs in a recent meta-analysis.

Here, we highlight some often overlooked assumptions in studies of APEs and provide a framework for identifying and testing APEs.

Our review highlights the importance of measuring environmental predictability, outlines the minimal requirements for experimental designs, explains the important differences between relative and absolute measures of offspring fitness, and highlights some potential issues in assigning components of offspring fitness to parental fitness.

Our recommendations should result in more targeted and effective tests of APEs.

Full paper

Burgess SC, Marshall DJ (2014) Adaptive parental effects: the importance of estimating  environmental predictability and offspring fitness appropriately PDFPDF 172 KB Oikos, 123: 769–776. doi: 10.1111/oik.01235

Adaptive maternal and paternal effects: gamete plasticity in response to parental stress

Authors: Natasha Jensen, Richard M Allen and Dustin J Marshall

Published in: Functional Ecology , volume 28, issue 3 (June 2014)


Transgenerational phenotypic plasticity is increasingly recognized as an important buffer of environmental change – many studies show that mothers alter the phenotype of their offspring so as to maximize their performance in their local environment. Fewer studies have examined the capacity of parents to alter the phenotype of their gametes to cope with environmental change. In organisms that shed their gametes externally, gametes are extremely vulnerable to local stresses and transgenerational plasticity in the phenotypes of gametes seems likely in this group.

In a marine tubeworm, Hydroides diramphus, we manipulated the salinity environment that mothers and fathers experienced before reproduction and then examined the phenotype of their gametes, as well as the performance of those gametes and the resultant larvae in different salinities.

We found strong evidence for gamete plasticity – both mothers and fathers adaptively adjust the phenotype of their gametes to maximize the performance of those gametes in the salinity regime experienced by their parents. Parents were quite flexible in the phenotype of gametes that they produced: they could switch the salinity tolerance of their gametes back and forth depending on their most recent experience.

Gamete plasticity was not without risks, however. We observed strong trade-offs in performance when gametes experienced an environment that did not match that of their parents. These effects of the parental environment persist for the duration of the larval phase such that larvae may not be able to disperse to environments that do not match their parents. Gamete plasticity may therefore represent an important source of phenotype–environment mismatches.

Gamete plasticity may represent an important mechanism for coping with environmental change and an important source of maternal and paternal effects in species with external fertilization. Studies that seek to predict the impacts of stresses that persist across generations (e.g. ocean acidification) should include parental exposures to the stress of interest.

Full paper

Jensen N, Allen RM, Marshall DJ (2014) Adaptive maternal and paternal effects: gamete plasticity in response to parental stress. Functional Ecology, 28: 724–733 PDFPDF 373 KB doi: 10.1111/1365-2435.12195

Faster is not always better: selection on growth rate fluctuates across life history and environments

Authors: Keyne Monro and Dustin J Marshall

Published in: The American Naturalist, volume 183, number 6 (June 2014)


Growth rate is increasingly recognized as a key life-history trait that may affect fitness directly rather than evolve as a by-product of selection on size or age.

An ongoing challenge is to explain the abundant levels of phenotypic and genetic variation in growth rates often seen in natural populations, despite what is expected to be consistently strong selection on this trait. Such a paradox suggests limits to how contemporary growth rates evolve.

We explored limits arising from variation in selection, based on selection differentials for age-specific growth rates expressed under different ecological conditions. We present results from a field experiment that measured growth rates and reproductive output in wild individuals of a colonial marine invertebrate (Hippopodina iririkiensis), replicated within and across the natural range of succession in its local community.

Colony growth rates varied phenotypically throughout this range, but not all such variation was available for selection, nor was it always targeted by selection as expected.

While the maintenance of both phenotypic and genetic variation in growth rate is often attributed to costs of growing rapidly, our study highlights the potential for fluctuating selection pressures throughout the life history and across environments to play an important role in this process.

Full paper

Monro K, Marshall DJ (2014) Faster isn’t always better: selection on growth rate fluctuates across the life history and environments. The American Naturalist, 183(6): 798–809 PDFPDF 393 KB doi:10.1086/676006

Circulation constrains the evolution of larval development modes and life histories in the coastal ocean

Authors: James M Pringle, James E Byers, Paula Pappalardo, John P Wares and Dustin J Marshall

Published in: Ecology, Volume 95, Issue 4 (April 2014)


The evolutionary pressures that drive long larval planktonic durations in some coastal marine organisms, while allowing direct development in others, have been vigorously debated. We introduce into the argument the asymmetric dispersal of larvae by coastal currents and find that the strength of the currents helps determine which dispersal strategies are evolutionarily stable.

In a spatially and temporally uniform coastal ocean of finite extent, direct development is always evolutionarily stable. For passively drifting larvae, long planktonic durations are stable when the ratio of mean to fluctuating currents is small and the rate at which larvae increase in size in the plankton is greater than the mortality rate (both in units of per time). However, larval behavior that reduces downstream larval dispersal for a given time in plankton will be selected for, consistent with widespread observations of behaviors that reduce dispersal of marine larvae. Larvae with long planktonic durations are shown to be favored not for the additional dispersal they allow, but for the additional fecundity that larval feeding in the plankton enables.

We analyzed the spatial distribution of larval life histories in a large database of coastal marine benthic invertebrates and documented a link between ocean circulation and the frequency of planktotrophy in the coastal ocean. The spatial variation in the frequency of species with planktotrophic larvae is largely consistent with our theory; increases in mean currents lead to a decrease in the fraction of species with planktotrophic larvae over a broad range of temperatures.

Full paper

Pringle JM, Byers JE, Pappalardo P, Wares JP, Marshall JP (2014) Circulation constrains the evolution of larval development modes and life histories in the coastal ocean. Ecology  95(4):1022–1032. PDFPDF 1.5 MB doi:10.1890/13-0970.1

Two sexes, one body: intra- and intersex covariation of gamete phenotypes in simultaneous hermaphrodites

Authors: Keyne Monro and Dustin J Marshall

Published in: Ecology and Evolution doi:10.1002/ece3.1035


By harboring male and female functions in the same genome and expressing them in every individual, simultaneous hermaphrodites may incur sexual conflict unless both sex functions can evolve phenotypic optima independently of each other.

The first step toward understanding their capacity to do so lies in understanding whether sex functions are phenotypically correlated within individuals, but remarkably few data address this issue.

We tested the potential for intra- and intersex covariation of gamete phenotypes to mediate sexual conflict in broadcast-spawning hermaphrodites (the ascidians Ciona intestinalis and Pyura praeputialis), for which sex-specific selection acts predominantly on sperm–egg interactions in the water column.

In both species, gamete phenotypes covaried within and across sex functions, implying that selection may be unable to target them independently because its direct effects on male gametes translate into correlated effects on female gametes and vice versa. This alone does not preclude the evolution of a different phenotypic optimum for each sex function, but imposes the more restrictive requirement that selection – which ultimately sorts among whole individuals, not sex functions – aligns with the direction in which gamete phenotypes covary at this level.

Full paper

Monro K, Marshall DJ (2014) Two sexes, one body: intra- and intersex covariation of gamete phenotypes in simultaneous hermaphrodites. Ecology and Evolution PDFPDF 274 KB doi:10.1002/ece3.1035