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

Initial offspring size mediates trade-off between fecundity and longevity in the field

Authors: Halil Kesselring, Rebecca Wheatley and Dustin J Marshall

Published in: Marine Ecology Progress Series, volume 465, doi: 10.3354/meps09865

Abstract

An understanding of the effects of intraspecific variation in offspring size is important from both an ecological and an evolutionary perspective.

While the relationship between off- spring size and overall offspring performance is key, most studies are restricted to examination of the effects of offspring size on early life-history stages only, and too few have examined the effects of offspring size throughout the life history.

Here, we examine the effects of offspring size on post- metamorphic survival, growth, and fecundity under field conditions for the polychaete Janua sp.

Larger offspring became larger adults and had higher levels of fecundity than those from smaller offspring, though the effect on fecundity was weaker and more variable over different experimental runs. Adults derived from larger larvae had shorter lifespans than adults derived from smaller larvae.

Our results suggest that the maternal effect of offspring size can influence the frequently observed trade-off between longevity and fecundity.

Future studies should seek to measure the effects of offspring size over as much of the life history as possible in order to avoid misestimating the relationship between offspring size and fitness.

Full paper

Kesselring H, Wheatley R, Marshall DJ (2012) Initial offspring size mediates trade-off between fecundity and longevity in the field. Marine Ecology Progress Series, 465: 129–136  email for a copy doi: 10.3354/meps09865

How do dispersal costs and habitat selection influence realized population connectivity?

Authors: Scott C Burgess, Eric A Treml and Dustin J Marshall

Published in: Ecology, volume 93, issue 6, doi: 10.1890/11-1656.1

Abstract

Despite the importance of dispersal for population connectivity, dispersal is often costly to the individual.

A major impediment to understanding connectivity has been a lack of data combining the movement of individuals and their survival to reproduction in the new habitat (realized connectivity).

Although mortality often occurs during dispersal (an immediate cost), in many organisms costs are paid after dispersal (deferred costs). It is unclear how such deferred costs influence the mismatch between dispersal and realized connectivity.

Through a series of experiments in the field and laboratory, we estimated both direct and indirect deferred costs in a marine bryozoan (Bugula neritina). We then used the empirical data to parameterize a theoretical model in order to formalize predictions about how dispersal costs influence realized connectivity.

Individuals were more likely to colonize poor-quality habitat after prolonged dispersal durations. Individuals that colonized poor-quality habitat performed poorly after colonization because of some property of the habitat (an indirect deferred cost) rather than from prolonged dispersal per se (a direct deferred cost).

Our theoretical model predicted that indirect deferred costs could result in nonlinear mismatches between spatial patterns of potential and realized connectivity.

The deferred costs of dispersal are likely to be crucial for determining how well patterns of dispersal reflect realized connectivity. Ignoring these deferred costs could lead to inaccurate predictions of spatial population dynamics.

Full paper

Burgess SC, Treml EA, Marshall DJ (2012) How do dispersal costs and habitat selection influence realized population connectivity? Ecology 93: 1378–1387 PDFPDF 622 KB doi: 10.1890/11-1656.1

Published paper: Minimal increase in genetic diversity enhances predation resistance

Authors: Kai S Koh, Carsten Matz, Chuan H Tan, Hoang L Le, Scott A Rice, Dustin J Marshall, Peter D Steinberg and Steffan Kjelleberg

Published in: Molecular Ecology, volume 21, issue 7, doi: 10.1111/j.1365-294X.2011.05415.x

Abstract

The importance of species diversity to emergent, ecological properties of communities is increasingly appreciated, but the importance of within-species genetic diversity for analogous emergent properties of populations is only just becoming apparent.

Here, the properties and effects of genetic variation on predation resistance in populations were assessed and the molecular mechanism underlying these emergent effects was investigated.

Using biofilms of the ubiquitous bacterium Serratia marcescens, we tested the importance of genetic diversity in defending biofilms against protozoan grazing, a main source of mortality for bacteria in all natural ecosystems.

S. marcescens biofilms established from wild-type cells produce heritable, stable variants, which when experimentally combined, persist as a diverse assemblage and are significantly more resistant to grazing than either wild type or variant biofilms grown in monoculture.

This diversity effect is biofilm-specific, a result of either facilitation or resource partitioning among variants, with equivalent experiments using planktonic cultures and grazers resulting in dominance by a single resistant strain.

The variants studied are all the result of single nucleotide polymorphisms in one regulatory gene suggesting that the benefits of genetic diversity in clonal biofilms can occur through remarkably minimal genetic change.

The findings presented here provide a new insight on the integration of genetics and population ecology, in which diversity arising through minimal changes in genotype can have major ecological implications for natural populations.

Full paper

Koh KS, Matz C, Tan CH, Le HL, Rice SA, Marshall DJ, Steinberg PP, Kjelleberg S (2012) Minimal increase in genetic diversity enhances predation resistance. Molecular Ecology 21: 1741–1753 PDFPDF 681 KB doi: 10.1111/j.1365-294X.2011.05415.x

Genetic diversity increases population productivity in a sessile marine invertebrate

Authors: J David Aguirre and Dustin J Marshall

Published in: Ecology, volume 93, issue 5, doi: 10.1890/11-1448.1

Abstract

Reductions in genetic diversity can have widespread ecological consequences: populations with higher genetic diversity are more stable, productive and resistant to disturbance or disease than populations with lower genetic diversity.

These ecological effects of genetic diversity differ from the more familiar evolutionary consequences of depleting genetic diversity, because ecological effects manifest within a single generation.

If common, genetic diversity effects have the potential to change the way we view and manage populations, but our understanding of these effects is far from complete, and the role of genetic diversity in sexually reproducing animals remains unclear.

Here, we examined the effects of genetic diversity in a sexually reproducing marine invertebrate in the field. We manipulated the genetic diversity of experimental populations and then measured individual survival, growth, and fecundity, as well as the size of offspring produced by individuals in high and low genetic diversity populations.

Overall, we found greater genetic diversity increased performance across all metrics, and that complementarity effects drove the increased productivity of our high-diversity populations.

Our results show that differences in genetic diversity among populations can have pervasive effects on population productivity within remarkably short periods of time.

Full paper

Aguirre JD, Marshall DJ (2012) Genetic diversity increases population productivity in a sessile marine invertebrate. Ecology 93: 1134–1142 PDFPDF 1.3 MB doi: 10.1890/11-1448.1

Advantages and disadvantages of interference-competitive ability and resource-use efficiency when invading established communities

Authors: Simon P Hart and Dustin J Marshall

Published in: Oikos, volume 121, issue 3, doi: 10.1111/j.1600-0706.2011.19557.x

Abstract

Invaders into established communities must overcome low resource availability. To establish, invaders must either appropriate resources from existing individuals through interference competition or efficiently use the small amount of resource that remains. Although both strategies may be important, they are rarely considered together and, in particular, resource-use efficiency is often ignored in systems dominated by interference competition.

To identify the traits that confer invasion success, we experimentally invaded resource patches in established communities with multiple species from two functional groups that differ in interference competitive ability and resource-use efficiency.

In contrast to previous assessments, we show that resource-use efficiency can facilitate invasion in systems dominated by interference competition. Furthermore, large resource requirements can be a liability when establishing because interference competition is inherently costly and so cannot fully compensate for limitations in the primary resource.However, we also show that there is a tradeoff in performance among functional groups between small and large resource gaps.

Our results suggest we modify the way we view and manage species invasion in systems dominated by interference competition.

Full paper

Hart SJ, Marshal DJ (2012) Advantages and disadvantages of interference-competitive ability and resource-use efficiency when invading established communities. Oikos, 121: 396–402 PDFPDF 132 KB doi: 10.1111/j.1600-0706.2011.19557.x

Does genetic diversity reduce sibling competition?

Authors: J. David Aguirre and Dustin J. Marshall

Published in: Evolution, volume 6, issue 1, doi: 10.1111/j.1558-5646.2011.01413.x

Abstract

An enduring hypothesis for the proximal benefits of sex is that recombination increases the genetic variation among offspring and that this genetic variation increases offspring performance. A corollary of this hypothesis is that mothers that mate multiply increase genetic variation within a clutch and gain benefits due to genetic diversity alone.

Many studies have demonstrated that multiple mating can increase offspring performance, but most attribute this increase to sexual selection and the role of genetic diversity has received less attention. Here, we used a breeding design to generate populations of full-siblings, half-siblings, and unrelated individuals of the solitary ascidian Ciona intestinalis. Importantly, we preclude the potentially confounding influences of maternal effects and sexual selection.

We found that individuals in populations with greater genetic diversity had greater performance (metamorphic success, postmetamorphic survival, and postmetamorphic size) than individuals in populations with lower genetic diversity. Furthermore, we show that by mating with multiple males and thereby increasing genetic variation within a single clutch of offspring, females gain indirect fitness benefits in the absence of mate-choice.

Our results show that when siblings are likely to interact, genetic variation among individuals can decrease competition for resources and generate substantial fitness benefits within a single generation.

Full paper

Aguirre JD, Marshall DJ (2012) Does genetic diversity reduce sibling competition? Evolution, 66-1: 94–102 PDFPDF 688 KB doi: 10.1111/j.1558-5646.2011.01413.x