The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate

Authors: Darren W Johnson, Keyne Monro, and Dustin J Marshall

Published in: Evolution, volume 67, issue 5 (May 2013)

Abstract

Why are sperm so variable despite having a singular, critical function and an intimate relationship with fitness?

A key to under-standing the evolution of sperm morphology is identifying which traits enable sperm to be successful fertilizers. Several sperm traits (e.g., tail length, overall size) are implicated in sperm performance, but the benefits of these traits are likely to be highly con- text dependent.

Here, we examined phenotypic selection on sperm morphology of a broadcast spawning tube worm (Galeolaria gemineoa). We conducted laboratory experiments to measure the relationship between average sperm morphology and relative fertilization success across a range of sperm environments that were designed to approximate the range of sperm concentrations and ages encountered by eggs in nature.

We found that the strength and form of multivariate selection varied substantially across our environmental gradients. Sperm with long tails and small heads were favored in high-concentration environments, whereas sperm with long heads were favored at low concentrations and old ages.

We suggest variation in the local fertilization environment and resulting differences in selection can preserve variability in sperm morphology both within and among males.

Full paper

Johnson D, Monro K, Marshall DJ (2013) The maintenance of sperm variability: context-dependent selection on sperm morphology in a broadcast spawning invertebrate. Evolution, 67-5: 1383–1395 PDF PDF 889 KB doi:10.1111/evo.12022

Competition in benthic marine invertebrates: the unrecognised role of exploitative competition for oxygen

Authors: Nick Ferguson, Craig R White and Dustin J Marshall

Published in: Ecology, volume 94, issue 1 (January 2013) doi: 10.1890/12-0795.1

Abstract

Competition is a ubiquitous structuring force across systems, but different fields emphasize the role of different types of competition.

In benthic marine environments, where some of the classic examples of competition were described, there is a strong emphasis on interference competition: marine invertebrates are assumed to compete fiercely for the limiting resource of space. Much of our understanding of the dynamics of this system is based on this assumption, yet empirical studies often find that increases in density can reduce performance despite free space being available. Furthermore, the assumption that space is the exclusively limiting resource raises paradoxes regarding species coexistence in this system.

Here, we measure the availability of oxygen in the field and in the laboratory, as well as the tolerance of resident species to low-oxygen conditions.

We show that oxygen can be the primary limiting resource in some instances, and that exploitative competition for this resource is very likely among benthic marine invertebrates. Furthermore, growth form (and the associated risk of oxygen limitation) covaries with the ability to withstand oxygen-poor conditions across a wide range of taxa.

Oxygen availability at very small scales may influence the distribution and abundance of sessile marine invertebrates more than is currently appreciated. Furthermore, competition for multiple resources (space and oxygen) and trade-offs in competitive ability for each may promote coexistence in this system.

Full paper

Ferguson N, White CR, Marshall DJ (2013) Competition in benthic marine invertebrates: the unrecognised role of exploitative competition for oxygen. Ecology, 94(1) 126–135 PDFPDF 311 KB 311 doi: 10.1890/12-0795.1

Costs of dispersal alter optimal offspring size in patchy habitats: combining theory and data for a marine invertebrate

Authors: Scott C Burgess, Michael Bode and Dustin J Marshall

Published in: Functional Ecology doi: 10.1111/1365-2435.12080

Abstract

Much of the theory on offspring size focuses on the effects of habitat quality on the relationship between offspring size and fitness. Habitat spacing may be another important factor that affects selection on offspring size when offspring disperse prior to colonization and accrue deferred costs that are mediated by offspring size.

We developed a theoretical model, based on a well-known optimality model, of how selection on offspring size changes with dispersal distance. The model assumes that offspring fitness depends on both offspring size and dispersal duration and that dispersal time and distance are positively related. Such assumptions are based on thousands of marine invertebrate species with non-feeding larvae, but our model also applies more generally to any organism where offspring size modifies the energetic costs of dispersal, and there is a positive relationship between dispersal duration and distance.

Our model predicts that, even when habitat quality does not vary, more isolated habitats may favour the production of fewer, larger offspring if smaller offspring incur greater deferred costs of dispersal. We then empirically demonstrate that offspring size and dispersal duration have interactive effects on post-settlement survival in a marine invertebrate (Bugula neritina), and such size-dependent deferred costs of dispersal are of a magnitude sufficient enough to potentially favour larger offspring in isolated habitats.

Together, our results indicate that the spatial pattern of suitable habitat could impose very different selective regimes on offspring size compared with the effects of habitat quality. Furthermore, our predictions contrast to those predicted for seed size and dispersal in plants, where the production of smaller, more numerous seeds is often a more efficient way for mothers to access distant, suitable habitat.

Full paper

Burgess SC, Bode M, Marshall DJ (2013) Costs of dispersal alter optimal offspring size in patchy habitats: combining theory and data for a marine invertebrate. Functional Ecology PDFPDF 329 KB doi: 10.1111/1365-2435.12080

Interspecific competition alters non-linear selection on offspring size in the field

Authors: Dustin J Marshall and Keyne Monro

Published in: Evolution, volume 67, issue 2 (February 2013) doi: 10.1111/j.1558-5646.2012.01749.x

Abstract

Offspring size is one of the most important life-history traits with consequences for both the ecology and evolution of most organisms. Surprisingly, formal estimates of selection on offspring size are rare, and the degree to which selection (particularly nonlinear selection) varies among environments remains poorly explored.

We estimate linear and nonlinear selection on offspring size, module size, and senescence rate for a sessile marine invertebrate in the field under three different intensities of interspecific competition. The intensity of competition strongly modified the strength and form of selection acting on offspring size.

We found evidence for differences in nonlinear selection across the three environments.

Our results suggest that the fitness returns of a given offspring size depend simultaneously on their environmental context, and on the context of other offspring traits. Offspring size effects can be more pervasive with regards to their influence on the fitness returns of other traits than previously recognized, and we suggest that the evolution of offspring size cannot be understood in isolation from other traits.

Overall, variability in the form and strength of selection on offspring size in nature may reduce the efficacy of selection on offspring size and maintain variation in this trait.

Full paper

Marshall DJ, Monro K (2013) Interspecific competition alters nonlinear selection on offspring size in the field. Evolution, 67-2: 328–337 PDFPDF 291 KB doi: 10.1111/j.1558-5646.2012.01749.x

Two PhD positions available: the ecology and/or evolutionary biology of sessile marine invertebrates (closed)

Update: applications are now closed.

Two fully-funded PhD stipends are available to students interested in working on the evolutionary ecology of sessile marine invertebrates in Dr Dustin Marshall’s Marine Evolutionary Ecology Group (MEEG). The specifics of the project will be a joint collaboration between student and supervisor.

The stipends include all course fees plus approximately $25,000 AUD per annum tax-free (the equivalent of approximately $33,000 AUD before tax) with no teaching requirements for 3.5 years (the length of a PhD in Australia).

I can guarantee funding of project costs and research support including the costs of attending at least one conference per year.

Project start dates can be any time in 2013.

Interested students should send their CVs, a brief statement of their interests and the contact details of two referees to dustin.marshall@monash.edu.

To be eligible, applicants must have completed at least one year of post-graduate research in ecology or evolution.

Preference will be given to those with strong quantitative skills and publications in international journals.

Applications close Monday 21 January 2013. Update: applications are now closed.

Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance

Authors: Angela J Crean, John M Dwyer and Dustin J Marshall

Published in: PLoS ONE, volume 7, issue 11, doi: 10.1371/journal.pone.0049167

Abstract

Styela plicata larvae

Styela plicata larvae. Image courtesy of Bronwyn Galletly.

Sperm are the most diverse cell type known: varying not only among- and within- species, but also among- and within- ejaculates of a single male.

Recently, the causes and consequences of variability in sperm phenotypes have received much attention, but the importance of within-ejaculate variability remains largely unknown.

Correlative evidence suggests that reduced within-ejaculate variation in sperm phenotype increases a male’s fertilization success in competitive conditions; but the transgenerational consequences of within-ejaculate variation in sperm phenotype remain relatively unexplored.

Here we examine the relationship between sperm longevity and offspring performance in a marine invertebrate with external fertilization, Styela plicata. Offspring sired by longer-lived sperm had higher performance compared to offspring sired by freshly-extracted sperm of the same ejaculate, both in the laboratory and the field. This indicates that within-ejaculate differences in sperm longevity can influence offspring fitness – a source of variability in offspring phenotypes that has not previously been considered. Links between sperm phenotype and offspring performance may constrain responses to selection on either sperm or offspring traits, with broad ecological and evolutionary implications.

Full paper

Crean AJ, Dwyer JM, Marshall DJ (2012) Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance. PLoS ONE 7 (11) PDFPDF 254 KB External linkFull text, doi: 10.1371/journal.pone.0049167

Revisiting the classic biogeographical patterns in marine invertebrate reproduction

After four years of data collection and over 4,000 papers, our paper revisiting the classic biogeographical patterns in marine invertebrate reproduction has been published here.

 Published paper: The biogeography of marine invertebrate life histories

Heat map of the distribution of studies used in the review to examine geographical variation in marine invertebrate life histories. The vast majority of the marine environment remains unstudied, and our view of marine life histories comes from only a small fraction of those studies that exist.

The biogeography of marine invertebrate life histories

Authors: Dustin J Marshall, Patrick J Krug, Elena K Kupriyanova, Maria Byrne and Richard B Emlet

Published in: Annual Review of Ecology, Evolution and Systematics, volume 43, pp. 97–114, doi: 10.1146/annurev-ecolsys-102710-145004

Abstract

Biologists have long sought to identify and explain patterns in the diverse array of marine life histories. The most famous speculation about such patterns is Gunnar Thorson’s suggestion that species producing planktonic larvae are rarer at higher latitudes (Thorson’s rule). Although some elements of Thorson’s rule have proven incorrect, other elements remain untested.

With a wealth of new life-history data, statistical approaches, and remote-sensing technology, new insights into marine reproduction can be generated.

We gathered life-history data for more than 1,000 marine invertebrates and examined patterns in the prevalence of different life histories. Systematic patterns in marine life histories exist at a range of scales, some of which support Thorson, whereas others suggest previously unrecognized relationships between the marine environment and the life histories of marine invertebrates.

Overall, marine life histories covary strongly with temperature and local ocean productivity, and different regions should be managed accordingly.

Full paper

Marshall DJ, Krug PJ, Kupriyanova EK, Byrne M, Emlet RB (2012) The biogeography of marine invertebrate life-histories. Annual Review of Ecology, Evolution and Systematics, 43: 97–114 External linke-print doi: 10.1146/annurev-ecolsys-102710-145004

Relatedness affects the density, distribution and phenotype of colonisers in four sessile marine invertebrates

Authors: J David Aguirre, Seth H Miller, Steven G Morgan and Dustin J Marshall

Published in: Oikos, Volume 122, issue 6 (June 2013) doi: 10.1111/j.1600-0706.2012.20827.x

Abstract

Genetic diversity has emerged as an important source of variation in the ecological properties of populations, but there are few studies of genetic diversity effects on colonisation processes. This relative scarcity of studies is surprising given the influence of colonisation on species coexistence, invasion, and population persistence.

Here, we manipulated relatedness in experimental populations of colonising larvae in four sessile marine invertebrates. We then examined the influence of coloniser relatedness on the number, spatial arrangement and phenotype of colonisers following permanent settlement. Overall, relatedness influenced colonisation in all four species, but the effects of relatedness on colonisation differed among species.

The variable responses of species to manipulations of relatedness likely reflect differences in intensity of inter- and intra-specific competition among adults, as well as the differential consequences of larval behaviours for each species. Relatedness appears to play an underappreciated role in the colonisation process, and we recommend that future studies of genetic diversity effects consider not only adult stages – the focus of most work to date – but also the importance of genetic diversity in early life history stages.

Full paper

Aguirre JD, Miller SH, Morgan SG, Marshal DJ (2012) Relatedness affects the density, distribution and phenotype of colonisers in four sessile marine invertebrates. Okios, 122: 881–888, 2013 PDFPDF 164 KB doi: 10.1111/j.1600-0706.2012.20827.x

Revisiting competition in a classic model system using formal links between theory and data

Authors: Simon P Hart, Jacqueline R Burgin and Dustin J Marshall

Published in: Ecology, volume 93, issue 9, doi: 10.1890/11-2248.1

Abstract

Formal links between theory and data are a critical goal for ecology. However, while our current understanding of competition provides the foundation for solving many derived ecological problems, this understanding is fractured because competition theory and data are rarely unified.

Conclusions from seminal studies in space-limited benthic marine systems, in particular, have been very influential for our general understanding of competition, but rely on traditional empirical methods with limited inferential power and compatibility with theory.

Here we explicitly link mathematical theory with experimental field data to provide a more sophisticated understanding of competition in this classic model system. In contrast to predictions from conceptual models, our estimates of competition coefficients show that a dominant space competitor can be equally affected by interspecific competition with a poor competitor (traditionally defined) as it is by intraspecific competition.

More generally, the often-invoked competitive hierarchies and intransitivities in this system might be usefully revisited using more sophisticated empirical and analytical approaches.

Full paper

Hart SP, Burgin JR, Marshall DJ (2012) Revisiting competition in a classic model system using formal links between theory and data. Ecology, 93(9) 2015–2022 PDFPDF 777 KB doi: 10.1890/11-2248.1