Environment-dependent variation in selection on life history across small spatial scales

Authors: Rolanda Lange, Keyne Monro and Dustin J Marshall

Published in: Evolution, volume 70, issue 10 (October 2016)

Abstract

Variation in life-history traits is ubiquitous, even though genetic variation is thought to be depleted by selection.

One potential mechanism for the maintenance of trait variation is spatially variable selection.

We explored spatial variation in selection in the field for a colonial marine invertebrate that shows phenotypic differences across a depth gradient of only 3 m. Our analysis included life-history traits relating to module size, colony growth, and phenology.

Directional selection on colony growth varied in strength across depths, while module size was under directional selection at one depth but not the other. Differences in selection may explain some of the observed phenotypic differentiation among depths for one trait but not another: instead, selection should actually erode the differences observed for this trait.

Our results suggest selection is not acting alone to maintain trait variation within and across environments in this system.

Citation

Lange R, Monro K, Marshall DJ (2016) Environment-dependent variation in selection on life history across small spatial scales, Evolution 70(10): 2404–2410 PDF 497 KB doi:10.1111/evo.13033

Dispersal duration mediates selection on offspring size

Authors: Karin Svanfeldt, Keyne Monro, and Dustin J Marshall

Published in: Oikos, volume 126, issue 4 (April 2017)

Abstract

Offspring size varies at all levels of organisation, among species, mothers and clutches. This variation is thought to be the result of a tradeoff between offspring quality and quantity, where larger offspring perform better but are more costly to produce. Local environmental conditions alter the benefits of increased offspring size and thereby mediate selection on this trait.

For sessile organisms, dispersal is a crucial part of the offspring phase, and in animals, bigger offspring tend to better endure longer dispersal distances than smaller offspring because they have more energy. Theory predicts that increasing distances between suitable habitats strengthens selection for larger offspring.

We manipulated the dispersal duration of offspring of different sizes in the bryozoan Watersipora subtorquata and then examined the relationship between offspring size and post-metamorphic performance in the field.

We found that selection on offspring size is altered by larval experience. Larger offspring had higher post-settlement performance if the larval period was short but, contrary to current theory, performed worse when the larval period was extended.

The reversal of the relationship between offspring size and performance by extending the larval phase in Watersipora may be due to the way in which offspring size affects growth in this species. Regardless of the mechanism, it appears that experiences in one life-history stage alter selection on offspring size in another stage, even when they occupy identical habitats as adults.

Citation

Svanfeldt K, Monro K, Marshall DJ (2017) Dispersal duration mediates selection on offspring size, Oikos, PDF 1 MB doi:10.1111/oik.03604

Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm

Authors: Keyne Monro and Dustin J Marshall

Published in: Proceedings of the Royal Society B, volume 283, issue 1834 (July 2016)

Abstract

Gamete dimorphism (anisogamy) defines the sexes in most multicellular organisms.

Theoretical explanations for its maintenance usually emphasize the size-related selection pressures of sperm competition and zygote survival, assuming that fertilization of all eggs precludes selection for phenotypes that enhance fertility. In external fertilizers, however, fertilization is often incomplete due to sperm limitation, and the risk of polyspermy weakens theadvantage of high sperm numbers that is predicted to limit sperm size, allowing alternative selection pressures to target free-swimming sperm.

We asked whether egg size and ejaculate size mediate selection on the free-swimming sperm of Galeolaria caespitosa, a marine tubeworm with external fertilization, by comparing relationships between sperm morphology and male fertility across manipulations of egg size and sperm density.

Our results suggest that selection pressures exerted by these factors may aid the maintenance of anisogamy in external fertilizers by limiting the adaptive value of larger sperm in the absence of competition. In doing so, our study offers a more complete explanation for the stability of anisogamy across the range of sperm environments typical of this mating system and identifies new potential for the sexes to coevolve via mutual selection pressures exerted by gametes at fertilization.

Citation

Monro K, Marshall DJ (2016) Unravelling anisogamy: egg size and ejaculate size mediate selection on morphology in free-swimming sperm, Proceedings of the Royal Society B, 283:1834 PDF 2.7 MB doi:10.1098/rspb.2016.0671

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

Quantifying the role of colonization history and biotic interactions in shaping communities – a community transplant approach

Authors: Chun-Yi Chang and Dustin J Marshall

Published in: Oikos, volume 126, issue 2 (February 2017)

Abstract

The role of colonization history and subsequent biotic interactions in determining the species composition in communities has long been the subject of debate in ecology. While one narrative has emphasized deterministic assembly rules, another has emphasized historical contingency.

One problem lies in approach: community studies are typically either manipulative but somewhat unnatural, or observational but lacking manipulation. Furthermore, while most ecologists now recognize that both historical and biotic factors shape communities, too few studies have moved beyond qualitative descriptions of their roles.

Here we use a manipulative approach that leverages natural variation to provide quantitative estimates of the relative contributions of colonization history and the subsequent biotic interactions. 384 communities were developed on artificial substrata in a homogeneous environment before undergoing reciprocal transplantation. We then compare community structure before and after transplantation as proxies for colonization history and biotic interactions.

We found that the importance of history and the ensuing biotic environment differed at different times in community development. Early transplantations resulted in the local environment modifying community history faster compared to postponed transplantations. With a four-week difference in age, colonization history explained 20% more of the variation in older communities than in younger communities. Biotic interactions were able to modify colonization history at the age of 16 weeks, but older communities showed more resistance to the changing biotic environment.

Our method provides a manipulative and quantitative approach for understanding the relative contributions of colonization history and biotic interactions to community in natural systems.

Citation

Chang CY, Marshall DJ (2017) Quantifying the role of colonization history and biotic interactions in shaping communities – a community transplant approach, Oikos, 126: 204–211 PDF 550 KB doi:10.1111/oik.03478

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

Biofilm history and oxygen availability interact to affect habitat selection in a marine invertebrate

Authors: Marcelo E Lagos, Craig R White and Dustin J Marshall

Published in: Biofouling, volume 32, issue 6

Abstract

In marine systems, oxygen availability varies at small temporal and spatial scales, such that current oxygen levels may not reflect conditions of the past.

Different studies have shown that marine invertebrate larvae can select settlement sites based on local oxygen levels and oxygenation history of the biofilm, but no study has examined the interaction of both.

The influence of normoxic and hypoxic water and oxygenation history of biofilms on pre-settlement behavior and settlement of the bryozoan Bugula neritina was tested. Larvae used cues in a hierarchical way: the oxygen levels in the water prime larvae to respond, the response to different biofilms is contingent on oxygen levels in the water. When oxygen levels varied throughout biofilm formation, larvae responded differently depending on the history of the biofilm.

It appears that B. neritina larvae integrate cues about current and historical oxygen levels to select the appropriate microhabitat and maximize their fitness.

Citation

Lagos ME, White CR, Marshall DJ (2016) Biofilm history and oxygen availability interact to affect habitat selection in a marine invertebrate, Biofouling, 32:6 645–655 PDF 1.6 MB doi: 10.1080/08927014.2016.1178725

Propagule size and dispersal costs mediate establishment success of an invasive species

Authors: Rolanda Lange and Dustin J Marshall

Published in: Ecology, volume 97, issue 3 (March 2016)

Abstract

Bio-invasions depend on the number and frequency of invaders arriving in new habitats. Yet, as is often the case, it is not only quantity that counts, but also quality.

The process of dispersal can change disperser quality and establishment success. Invasions are a form of extra-range dispersal, so that invaders often experience changes in quality through dispersal.

To study effects of dispersal on invader quality, and its interactions with quantity on invasion success, we manipulated both in a field experiment using an invasive marine invertebrate.

Establishment success increased with the number of individuals arriving in a new habitat. Prolonged larval durations – our manipulation of prolonged dispersal – decreased individual quality and establishment success. Groups of invaders with prolonged larval durations contributed only a third of the offspring relative to invaders that settled immediately.

We also found an interaction between the quality and quantity of invaders on individual growth: only within high-quality cohorts did individuals experience density-dependent effects on growth.

Our findings highlight that dispersal not only affects the quantity of invaders arriving in a new habitat but also their quality, and both mediate establishment success.

Citation

Lange R , Marshall DJ (2016) Propagule size and dispersal costs mediate establishment success of an invasive species. Ecology, 97(3), 2016, pp. 569–575
DOI: 10.1890/15-1573 PDF 238 KB

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