Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification

Authors: Juan Diego Gaitán-Espitia, Dustin Marshall, Sam Dupont, Leonardo D Bacigalupe, Levente Bodrossy and Alistair J Hobday

Published in: Biology Letters, volume 13, issue 2 (February 2017)

Abstract

Geographical gradients in selection can shape different genetic architectures in natural populations, reflecting potential genetic constraints for adaptive evolution under climate change.

Investigation of natural pH/pCO₂ variation in upwelling regions reveals different spatio-temporal patterns of natural selection, generating genetic and phenotypic clines in populations, and potentially leading to local adaptation, relevant to understanding effects of ocean acidification (OA).

Strong directional selection, associated with intense and continuous upwellings, may have depleted genetic variation in populations within these upwelling regions, favouring increased tolerances to low pH but with an associated cost in other traits. In contrast, diversifying or weak directional selection in populations with seasonal upwellings or outside major upwelling regions may have resulted in higher genetic variances and the lack of genetic correlations among traits.

Testing this hypothesis in geographical regions with similar environmental conditions to those predicted under climate change will build insights into how selection may act in the future and how populations may respond to stressors such as OA.

Citation

Gaitán-Espitia JD, Marshall D, Dupont S, Bacigalupe LD, Bodrossy L, Hobday AJ (2017) Geographical gradients in selection can reveal genetic constraints for evolutionary responses to ocean acidification. Biology Letters, 13(2) 20160784. LINK
doi: 10.1098/rsbl.2016.0784

Limited evolutionary responses to harvesting regime in the intensive production of algae

Authors: Rebecca J Lawton, Nicholas A Paul, Dustin J Marshall and Keyne Monro

Published in: Journal of Applied Phycology, January 2016

Abstract

Plastic changes in the growth and productivity of algae in response to environment and stocking density are well established. In contrast, the capacity for such changes to persist once environmental differences cease, potentially signalling an evolutionary response, have rarely been tested for algae in intensive production systems.

We tested whether continuous differences in harvesting regime (a high stocking density/low-yield regime versus low stocking density/high-yield regime) generated changes in biomass productivity and other growth metrics within several strains of the clonal macroalga Oedogonium (Chlorophyta, Oedogoniales) and whether such changes persisted once differential harvesting yields ceased.

We found considerable plasticity in growth rate and biomass productivity over a 12-week period of active selection (i.e. repeated high-yield and low-yield harvesting of clonal lineages within strains) and that strains responded differently to this selection pressure over time.

While small, but significant, differences in growth rates of clonal lineages exposed to high-yield vs low-yield harvesting regimes were maintained after prolonged culture under a common selection regime (i.e. medium-yield harvesting), differences in biomass productivity were not. There was no evidence for positive or negative effects of maintaining multiple strains in polyculture on growth and biomass productivity.

Overall, we detected limited potential for evolutionary responses to harvesting regime in the main commercial trait of interest — biomass productivity. This outcome is important for commercial cultivation in intensive production systems, since it identifies a low risk that harvesting practices will impact negatively on biomass productivity in the longer term.

Citation

Lawton RJ, Paul NA, Marshall DJ, Monro K (2017) Limited evolutionary responses to harvesting regime in the intensive production of algae. Journal of Applied Phycology PDF 1 MB doi:10.1007/s10811-016-1044-8

Temperature effects on mass-scaling exponents in colonial animals: a manipulative test

Authors: Diego R Barneche, Craig R White and Dustin J Marshall

Published in: Ecology, volume 98, issue 1 (January 2017)

Abstract

Body size and temperature are fundamental drivers of ecological processes because they determine metabolic rates at the individual level. Whether these drivers act independently on individual-level metabolic rates remains uncertain.

Most studies of intraspecic scaling of unitary organisms must rely on pre-existing differences in size to examine its relationship with metabolic rate, thereby potentially confounding size-correlated traits (e.g., age, nutrition) with size, which can affect metabolic rate.

Here, we use a size manipulation approach to test whether metabolic mass scaling and temperature dependence interact in four species (two phyla) of colonial marine invertebrates. Size manipulation in colonial organisms allows tests of how ecological processes (e.g., predation) affect individual physiology and consequently population- and community-level energy flux.

Body mass and temperature interacted in two species, with one species exhibiting decreased and the other increased mass-scaling exponents with increasing temperature.

The allometric scaling of metabolic rate that we observe in three species contrasts with the isometric scaling of ingestion rates observed in some colonial marine invertebrates.

Thus, we suggest that the often observed competitive superiority of colonial over unitary organisms may arise because the difference between energy intake and expenditure increases more strongly with size in colonial organisms.

Citation

Barneche DR, White CR, Marshall DJ (2016) Temperature effects on mass-scaling exponents in colonial animals: a manipulative test, Ecology, 98(1), 2017, pp. 103–111 PDF 534 KB doi:10.1002/ecy.1624

Why do larger mothers produce larger offspring? A test of classic theory

Authors: Hayley Cameron, Keyne Monro, Martino Malerba, Stephan Munch and Dustin Marshall

Published in: Ecology, volume 97, issue 12 (December 2016)

Abstract

Across a wide range of taxa, larger mothers produce larger offspring.

Theory assumes that larger, more fecund mothers create higher local densities of siblings, and so larger mothers produce larger offspring to offset sibling competition. This assumption has been debated for over 30 years, but direct empirical tests are surprisingly rare.

Here, we test two key assumptions of classic theories that predict sibling competition drives maternal-size–offspring-size (MSOS) correlations:

  1. independent effects of offspring size and sibling density on offspring performance or
  2. as a product of an interaction between these two factors.

To simultaneously test these alternative assumptions, we manipulate offspring size and sibling density in the marine invertebrate, Bugula neritina, and monitor offspring performance in the field.

We found that, depending on the fitness metric being considered, offspring size and sibling density can either independently or interactively affect offspring performance. Yet sibling density did not affect offspring performance in the ways that classic theories assume.

Given our results, it is unlikely that sibling competition drives the positive MSOS correlation observed in this species. Empirical support for these classic theories remains lacking, suggesting alternative explanations are necessary.

Citation

Cameron H, Monro K, Malerba M, Munch S, Marshall DJ (2016) Why do larger mothers produce larger offspring? A test of classic theory. Ecology, 97: 3452–3459. PDF 415 KB doi:10.1002/ecy.1590

Spatial pattern of distribution of marine invertebrates within a subtidal community: do communities vary more among patches or plots?

Authors: Chun‐Yi Chang and Dustin J Marshall

Published in: Ecology and Evolution, volume 6, issue 22 (November 2016)

Abstract

Making links between ecological processes and the scales at which they operate is an enduring challenge of community ecology.

Our understanding of ecological communities cannot advance if we do not distinguish larger scale processes from smaller ones.

Variability at small spatial scales can be important because it carries information about biological interactions, which cannot be explained by environmental heterogeneity alone.

Marine fouling communities are shaped by both the supply of larvae and competition for resources among colonizers—these two processes operate on distinctly different scales.

Here, we demonstrate how fouling community structure varies with spatial scale in a temperate Australian environment, and we identify the spatial scale that captures the most variability. Community structure was quantified with both univariate (species richness and diversity) and multivariate (similarity in species composition) indices.

Variation in community structure was unevenly distributed between the spatial scales that we examined. While variation in community structure within patch was usually greater than among patch, variation among patch was always significant.

Opportunistic taxa that rely heavily on rapid colonization of free space spread more evenly among patches during early succession. In contrast, taxa that are strong adult competitors but slow colonizers spread more evenly among patches only during late succession.

Our findings show significant patchiness can develop in a habitat showing no systematic environmental spatial variation, and this patchiness can be mediated through different biological factors at different spatial scales.

Citation

Chang CY, Marshall DJ (2016) Spatial pattern of distribution of marine invertebrates within a subtidal community: do communities vary more among patches or plots? Ecology and Evolution 6(22)83308337 PDF 522 KB doi: 10.1002/ece3.2462

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

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

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