Global change, life-history complexity and the potential for evolutionary rescue

Authors: Dustin J Marshall, Scott C Burgess and Tim Connallon

Published in: Evolutionary Applications, May 2016

Abstract

Most organisms have complex life cycles, and in marine taxa, larval life-history stages tend to be more sensitive to environmental stress than adult (reproductive) life-history stages.

While there are several models of stage-specific adaptation across the life history, the extent to which differential sensitivity to environmental stress (defined here as reductions in absolute fitness across the life history) affects the tempo of adaptive evolution to change remains unclear.

We used a heuristic model to explore how commonly observed features associated with marine complex life histories alter a population’s capacity to cope with environmental change.

We found that increasing the complexity of the life history generally reduces the evolutionary potential of taxa to cope with environmental change. Our model also predicted that genetic correlations in stress tolerance between stages, levels of genetic variance in each stage, and the relative plasticity of different stages, all interact to affect the maximum rate of environmental change that will permit species persistence.

Our results suggest that marine organisms with complex life cycles are particularly vulnerable to anthropogenic global change, but we lack empirical estimates of key parameters for most species.

Citation

Marshall DJ, Burgess SC, Connallon T (2016) Global change, life-history complexity and the potential for evolutionary rescue, Evolutionary ApplicationsPDF 434 KB doi:10.1111/eva.12396

Metabolic rate covaries with fitness and the pace of the life history in the field

Authors: Amanda K Pettersen, Craig R White and Dustin J Marshall

Published in: Proceedings of the Royal Society B, volume 283, issue 1831 (May 2016)

Abstract

Metabolic rate reflects the ‘pace of life’ in every organism. Metabolic rate is related to an organism’s capacity for essential maintenance, growth and reproduction—all of which interact to affect fitness.

Although thousands of measurements of metabolic rate have been made, the microevolutionary forces that shape metabolic rate remain poorly resolved. The relationship between metabolic rate and components of fitness are often inconsistent, possibly because these fitness components incompletely map to actual fitness and often negatively covary with each other.

Here we measure metabolic rate across ontogeny and monitor its effects on actual fitness (lifetime reproductive output) for a marine bryozoan in the field. We also measure key components of fitness throughout the entire life history including growth rate, longevity and age at the onset of reproduction.

We found that correlational selection favours individuals with higher metabolic rates in one stage and lower metabolic rates in the other—individuals with similar metabolic rates in each developmental stage displayed the lowest fitness. Furthermore, individuals with the lowest metabolic rates lived for longer and reproduced more, but they also grew more slowly and took longer to reproduce initially.

That metabolic rate is related to the pace of the life history in nature has long been suggested by macroevolutionary patterns but this study reveals the microevolutionary processes that probably generated these patterns.

Citation

Pettersen A, White CF, Marshall DJ (2016) Metabolic rate covaries with fitness and the pace of the life history in the field, Proceedings of the Royal Society B, 283: 20160323
PDF 548 KB doi: 20160323. doi:10.1098/rspb.2016.0323

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)

Abstract

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.

Citation

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

Relative contributions of offspring quality and environmental quality to adult field performance

Authors: Rolanda Lange and Dustin J Marshall

Published in: Oikos, volume 125,  issue 2 (February 2016)

Abstract

Determinants of adult performance, such as growth and survival, are influenced by extrinsic, environmental and intrinsic, phenotypic factors. The relative importance of extrinsic and intrinsic factors, while ecologically relevant, is rarely estimated simultaneously.

We estimate the relative contributions of offspring size (intrinsic) and various environmental factors (extrinsic) on adult performance in the marine colonial bryozoan Watersipora subtorquata.

We used a variance partitioning approach for both new and previously published data, enabling us to examine the performance of over 1000 individuals in the field.

We found offspring size to explain relatively little variation in adult performance. Of the environmental factors taken to account, temporal variation and an environmental gradient had the strongest influences.

Citation

Lange R, Marshall DJ (2016) Relative contributions of offspring quality and environmental quality to adult field performance, Oikos 125: 210–217, 2016 PDF 1.3 MB doi:10.1111/oik.02473

How not to influence ecology: three things we have learned at Oikos

Authors: Dustin J Marshall and Dries Bonte

Published in: Oikos, volume 125, issue 1 (January 2016)

Here at OIKOS, we receive around five or six proposals for a Forum article every week. The Forum is a place where ecological ideas can be kicked around and examined from a different angle. Our hope is that some will provide a high level of synthesis in the field of ecology.

The Forum is a place where ecological ideas can be kicked around and examined from a different angle. Our hope is that some will provide a high level of synthesis in the field of ecology.

Some of the best papers that we’ve had the privilege to handle as an editor have been Forum papers and we believe that the Forum plays a very important role in OIKOS, and a role in the field of ecology more generally. For that reason, we love the chance to handle great Forum papers. We really dislike the other part of our job: rejecting most of the Forum proposals we get each week. Here, we thought we should provide some insights into why most proposals get rejected.

We really dislike the other part of our job: rejecting most of the Forum proposals we get each week. Here, we thought we should provide some insights into why most proposals get rejected.

Necessity

While we get Forum pieces on many, many topics, a single feature unites the best ones: the author felt compelled to write it. The most effective Forum pieces are those that the author felt just had to be written, that the field was limping along under a misguided principle, that key principles were misunderstood, or despite what the field thought it knew, it actually didn’t. Those proposals where the author fiercely believes that ecology won’t be as effective as it could be with-out the Forum paper are the ones that are, in my view, the best. We remember one proposal in particular that basically said, “I really didn’t want to write this thing but the field keeps messing this thing up so I had no choice”. The

We remember one proposal in particular that basically said, “I really didn’t want to write this thing but the field keeps messing this thing up so I had no choice”. The resulting article was an excellent contribution that changed the field for the better. In contrast, many other proposals, while they have something to say, are basically tracking along with the field and it is unclear that the field actually needs a Forum piece in order to move forward. One issue here is the

One issue here is the pressure for graduate students to accumulate papers as quickly as possible, which leads to the submission of thesis summaries as Forum proposals. In our experience at OIKOS, many of these proposals are adept summaries of the field, but generally are not suitable as Forum pieces as they rarely provide synthesis.

Telling rather than showing

We get many, many submissions proposing a new framework / model system / approach where the purpose of the Forum article would be to draw attention to a particular thing that the author believes is valuable. We have published such papers over the years and

We have published such papers over the years and they almost universally fail to have much influence on the field. We suspect that the reason for

We suspect that the reason for lack of traction: there are lots of approaches / frameworks / model systems out there, an overwhelming number actually. In response to this overwhelming number, most researchers use approaches or model systems or frameworks that have been shown to work very well.

A model system becomes a model system because some brave soul shows the world the power of such a system through excellent empiricism. An approach is taken up more widely when researchers show that it allows unprecedented access to a particular problem via a series of experiments.

You may feel that your particular approach is superior, or that your framework is the absolute best for tackling a problem, you may also be right but scientists are rather conservative. Scientists will not take something up just because you tell them it is the right thing to do; instead you have to show them, through your own work.

One paper (however good) is unlikely to change a field’s whole approach to a problem, so you have to be patient. Through repeated demonstration in your own empiricism, show that your framework (or approach, or model system) is actually best.

The uptake of a new approach takes time, it is idiosyncratic, probably biased towards established academics, and unfortunately, probably biased geographically (we are guessing here but we suspect that if someone utilises a new method in California, it is more likely to catch on than if the same method was discovered in Peru).

So we see the appeal of writing a Forum piece to catalyse the uptake of some great new thing.

The problem is, we rarely see such an approach succeed. At the very least, ecologists are likely to be wary of a new thing until they see the proponents of the thing successfully tackle a range of problems themselves.

So, trust that science is an (imperfect) meritocracy, your great ideas will shine through and be taken up by the field if you persist with them.

Overall, we think this issue can be best summed up with a (paraphrased) Twain quote:

“Don’t say the person screamed. Bring them on and let them scream.”

They said something mean about my field or paper

As a scientist, it is infuriating when someone else misrepresents one’s work. It can also be very confronting to have key premises of a field challenged, or dismissed.

We receive many Forum proposals that seek to respond to such challenges or attacks.

We wrote about this problem around four years ago on the OIKOS blog and the issue has not gone away. We do not publish such exchanges in OIKOS as we have not seen much evidence that they are productive. We recognise this will be exasperating for many given that we occasionally publish heretical Forum pieces and then do not provide the opportunity for others to respond in kind. We note that no one has managed to obliterate a field via a Forum article so far and we doubt that they ever will. So, if you truly disagree with a Forum article, show through empiricism that it is incorrect. Hold your fire, instead use empiricism to make your point.

These three suggestions will seem opaque to some, offensive to others, and obvious to most. Nevertheless, we suspect that editors for other journals will recognise some of these same issues, and may agree (we would love to hear from them either way).

Our hope in writing this editorial is that authors avoid wasting their time with doomed proposals. Our key suggestion is for authors to ask themselves, “How would I react to my proposed Forum piece if it were not written by me? Would I change the way I thought about, or did ecology?” If the answer is yes, then go ahead. We look forward to reading it.

Citation

Marshall DJ, Bonte D (2016) How not to influence ecology: three things we have learned at Oikos. Oikos, 125: 1–2, 2016 PDF 472 KB doi: 10.1111/oik.03107 doi:10.1111/oik.03107

Why does offspring size affect performance? Integrating metabolic scaling with life-history theory

Authors: Amanda K Pettersen, Craig R White and Dustin J Marshall

Published in: Proceedings of the Royal Society B, volume 282, issue 1819 (November 2015)

Abstract

Within species, larger offspring typically out-perform smaller offspring. While the relationship between offspring size and performance is ubiquitous, the cause of this relationship remains elusive.

By linking metabolic and life-history theory, we provide a general explanation for why larger offspring perform better than smaller offspring. Using high-throughput respirometry arrays, we link metabolic rate to offspring size in two species of marine bryozoan.

We found that metabolism scales allometrically with offspring size in both species: while larger offspring use absolutely more energy than smaller offspring, larger offspring use proportionally less of their maternally derived energy throughout the dependent, non-feeding phase. The increased metabolic efficiency of larger offspring while dependent on maternal investment may explain offspring size effects—larger offspring reach nutritional independence (feed for themselves) with a higher proportion of energy relative to structure than smaller offspring.

These findings offer a potentially universal explanation for why larger offspring tend to perform better than smaller offspring but studies on other taxa are needed.

Citation

Pettersen AK, White CR, Marshall DJ (2015) Why does offspring size affect performance? Integrating metabolic scaling with life-history theory. Proceedings of the Royal Society B, 282: 20151946. PDF 771 KB LINK doi:10.1098/rspb.2015.1946

Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicate (Ascidiaceae)

Authors: Angela J Crean and Dustin J Marshall

Published in: Marine Biology, volume 162, issue 11 (November 2015)

Abstract

The evolution of egg size has been intensively studied due to its influence on both fecundity and offspring performance. In marine broadcast spawners, egg size influences the probability of sperm–egg collision, and therefore, egg size can also in influence fertilization success, depending on the local concentration of sperm.

Many broadcast-spawning species have egg accessory structures that are thought to be a cheap means of altering egg size, but their influence on fertilization remains controversial.

To determine the relative influences of ovicell size and follicle cell size on fertilization success in the ascidian Styela plicata, the size distribution of eggs that were not successfully fertilized in both high and low sperm concentrations was compared to that of unfertilized controls.

At high sperm concentrations, a greater proportion of eggs with smaller ovicells were fertilized, resulting in smaller larvae hatching from this treatment. Eggs with a large follicle cell area relative to ovicell area were preferentially fertilized in both high and low sperm concentration treatments.

Hence, follicle cells do not eliminate selection on ovicell size at fertilization in S. plicata. Furthermore, follicle cells appear to increase fertilization success across a range of sperm concentrations by performing different functions in each environment — increasing the target size of eggs in low-sperm concentrations and presumably reducing polyspermy in high sperm concentrations.

Citation

Crean AJ, Marshall DJ (2015) Eggs with larger accessory structures are more likely to be fertilized in both low and high sperm concentrations in Styela plicata (Ascidiaceae). Marine Biology, 162:2251–2256 PDF 318 KB doi:10.1007/s00227-015-2755-0

Evolutionary consequences of fertilization mode for reproductive phenology and asynchrony

Authors: Colin Olito, Michael Bode and Dustin J Marshall

Published in: Marine Ecology Progress Series, volume 537

Abstract

Reproductive phenology is a crucial life-history trait that is influenced by both environmental and frequency-dependent effects. The fitness benefits of any phenology strategy will depend strongly on other aspects of the life history: one of the most fundamental ways life histories can differ is fertilization mode. Despite the strong potential for fertilization mode to alter selection on phenology, explorations into how these 2 fundamental life-history traits interact are lacking.

We explore theoretically how frequency-dependent effects and fertilization mode influence the evolution of asynchronous reproduction, and the evolutionary stable strategy (ESS) for a population in which individuals’ mean and variance in phenology are evolvable traits.

We find that when males compete for fertilizations, perfect reproductive synchrony with optimal environmental conditions is never an optimal evolutionary strategy, and asynchronous reproduction is an inevitable consequence of frequency-dependent selection. Fertilization mode qualitatively alters frequency-dependent selection on the variance in phenology, as well as the prevalence of sexual conflict over reproductive timing.

Our results contrast with traditional hypotheses that have primarily considered asynchronous reproduction as an adaptive bet-hedging strategy in stochastic environments, and provide a much-needed explanation for the emerging picture of reproductive asynchrony observed in many systems.

Citation

Olito C, Bode M, Marshall DJ (2015) Evolutionary consequences of fertilization mode for reproductive phenology and asynchrony. Marine Ecology Progress Series, 537: 23–38 PDF 491 KB doi: 10.3354/meps11453

 

The biogeography of fertilization mode in the sea

Authors: Keyne Monro and Dustin J Marshall

Published in: Global Ecology and Biogeography, volume 24, issue 12 (December 2015)

Abstract

Knowledge of the biogeography of life histories is central to understanding and predicting the impacts of global change on key functional traits that shape species distributions and transcend taxonomic boundaries. Whether species are internal or external fertilizers is a fundamental aspect of reproductive diversity in the sea, and has profound ecological and evolutionary consequences. However, geographic variation in this trait and the factors that potentially drive it (e.g. transitions in associated life-history traits, ecological conditions that favour one mode over the other or the evolutionary history of species) remain poorly characterized.

We collated life-history data (modes of fertilization and development), geographic data and biophysical data (sea-surface temperatures and food availability) for 1532 marine species spanning 17 invertebrate phyla. We used standard and phylogenetic logistic regressions to evaluate latitudinal gradients in fertilization mode, plus their interactions with development (transitions from planktonic to aplanktonic development, or from feeding to non-feeding larvae) and taxonomy. We also explored the dependence of fertilization mode on biophysical variables to understand how ecology potentially contributes to geographic variation in this trait.

Fertilization mode often varies predictably with latitude, but the exact nature of this relationship depends on developmental mode and the phylum under consideration. Some commonalities were evident, however, with the likelihood of internal fertilization declining at higher latitudes for Annelida and Echinodermata with aplanktonic development, but increasing at higher latitudes for Cnidaria and Porifera with non-feeding, planktonic larvae. Synergistic effects of temperature and food availability may potentially shape some of these patterns.

There are latitudinal gradients in fertilization mode in the sea. The variation among phyla and developmental modes, however, is a complexity that is unexplained by existing theory. Combined effects of recent adaptation and deeper phylogenetic history have probably shaped this systematic variation in the reproductive ecology of marine organisms.

Citation

Monro K, Marshall DJ (2015) The biogeography of fertilization mode in the sea. Global Ecology and Biogeography, 24: 1499–1509 PDF 534 KB doi: 10.1111/geb.12358

Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?

Authors: Annie S Guillaume, Keyne Monro and Dustin J Marshall

Abstract

For most organisms, early life-history stages are the most sensitive to environmental stress and so transgenerational phenotypic plasticity, whereby the parental environment and off-spring environment interact to alter the phenotype of the offspring, is viewed as key to promoting
persistence in the face of environmental change. While there has been long-standing interest in the role of transgenerational plasticity via the maternal line (traditionally the field of maternal effects), increasingly it appears that paternal effects can also play a role.

Despite the emerging role of paternal effects in studies of global change, key knowledge gaps remain: first, whether paternal effects act to increase or decrease offspring performance remains largely unexplored; second, the relative roles of maternal and paternal effects are rarely disentangled; and third, the role of environmental variation, a key determinant of the
benefits of transgenerational plasticity, has not been explored with regard to paternal effects.

Here, we explore all three issues using the marine tubeworm Galeolaria caespitosa, an important habitat-forming species in southern Australia.

We found that both paternal and maternal experiences affected key stages of offspring performance (fertilization and larval development) and, surprisingly, paternal effects were often stronger than maternal effects. Furthermore, we found that paternal effects often reduced off-spring performance, especially when environments varied compared with when environments were stable.

Our results suggest that, while transgenerational plasticity may play an important role in modifying the impacts of global change, these effects are not uniformly positive. Importantly, paternal effects can be as strong, or stronger, than maternal effects and environmental variability
strongly alters the impacts of paternal effects.

Citation

Guillaume AS, Monro K, Marshall DJ (2015) Transgenerational plasticity and environmental stress: do paternal effects act as a conduit or a buffer?, Functional Ecology PDF 397 KB doi:10.1111/1365-2435.12604