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)

Abstract

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 http://dx.doi.org/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)

Abstract

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)

Abstract

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)

Abstract

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)

Abstract

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

Abstract

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

Offspring size in a resident species affects community assembly

Authors: Kurt Davis and Dustin J Marshall

Published in: Journal of Animal Ecology, volume 83, issue 2 (March 2014)

Abstract

Offspring size is a trait of fundamental importance that affects the ecology and evolution of a range of organisms. Despite the pervasive impact of offspring size for those offspring, the influence of offspring size on other species in the broader community remains unexplored. Such community-wide effects of offspring size are likely, but they have not been anticipated by theory or explored empirically.

For a marine invertebrate community, we manipulated the size and density of offspring of a resident species (Watersipora subtorquata) in the field and examined subsequent community assembly around that resident species.

Communities that assembled around larger offspring were denser and less diverse than communities that assembled around smaller offspring. Differences in niche usage by colonies from smaller and larger offspring may be driving these community-level effects.

Our results suggest that offspring size is an important but unexplored source of ecological variation and that life-history theory must accommodate the effects of offspring size on com- munity assembly. Life-history theory often assumes that environmental variation drives intra- specific variation in offspring size, and our results show that the converse can also occur.

Full paper

Davis K, Marshall DJ (2014) Offspring size in a resident species affects community assembly. Journal of Animal Ecology, 83, 322–331 PDF PDF 274 KB doi:10.1111/1365-2656.12136

Environmental stress, facilitation, competition, and coexistence

Authors: Simon P Hart and Dustin J Marshall

Published in: Ecology, volume 94, issue 12 (December 2013)

Abstract

The major theories regarding the combined influence of the environment and species interactions on population and community dynamics appear to conflict.

Stress/disturbance gradient models of community organization, such as the stress gradient hypothesis, emphasize a diminished role for competition in harsh environments whereas modern coexistence theory does not.

Confusion about the role of species interactions in harsh environments is perpetuated by a disconnect between population dynamics theory and data.

We linked theory and data using response surface experiments done in the field to parameterize mathematical, population-dynamic competition models. We replicated our experiment across two environments that spanned a common and important environmental stress gradient for determining community structure in benthic marine systems. We generated quantitative estimates of the effects of environmental stress on population growth rates and the direction and strength of intra- and interspecific interactions within each environment.

Our approach directly addressed a perpetual blind spot in this field by showing how the effects of competition can be intensified in stressful environments even though the apparent strength of competition remains unchanged.

Furthermore, we showed how simultaneous, reciprocal competitive and facilitative effects can stabilize population dynamics in multispecies communities in stressful environments.

Full paper

Hart SP, Marshall DJ (2013) Environmental stress, facilitation, competition and coexistence. Ecology, 94(12): 2719–2731 PDFPDF 1.7 MB doi:10.1890/12-0804.1

Evolutionary constraints and the maintenance of individual specialization throughout succession

Authors: Keyne Monro and Dustin J Marshall

Published in: Evolution, volume 67, issue 12 (December 2013)

Abstract

Constraints on life-history traits, with their close links to fitness, are widely invoked as limits to niche expansion at most organiza- tional levels.

Theoretically, such constraints can maintain individual specialization by preventing adaptation to all niches available, but empirical evidence of them remains elusive for natural populations. This problem may be compounded by a tendency to seek constraints involving multiple traits, neglecting their added potential to manifest in trait expression across environments (i.e., within reaction norms).

By replicating genotypes of a colonial marine invertebrate across successional stages in its local community, and taking a holistic approach to the analysis of ensuing reaction norms for fitness, we show the potential for individual specialization to be maintained by genetic constraints associated with these norms, which limit the potential for fitness at one successional stage to improve without loss of fitness at others.

Our study provides new insight into the evolutionary maintenance of individual specialization in natural populations and reinforces the importance of reaction norms for studying this phenomenon.

Full paper

Monro K, Marshall DJ (2013) Evolutionary constraints and the maintenance of individual specialization throughout succession. Evolution 67(12): 3676–3644 PDFPDF 495 KB doi:10.1111/evo.12220

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)

Abstract

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