Debating growth and reproduction

In a recent post we described a paper written by Dustin Marshall and Craig White and published in Trends in Ecology and Evolution (TREE). The published article was called “Have we outgrown the existing models of growth?” In it, Dustin and Craig suggest that the growth dynamics that biologists have long sought to understand probably emerge simply from hyperallometric scaling of reproduction.

Daniel Pauly is a fisheries scientist from the University of British Columbia and is a proponent of the Gill-Oxygen Limitation Theory (GOLT) of growth. This theory applies to water-breathing animals and is structured around the proposition that growth is necessarily constrained by the size of the gills and the oxygen they are able to extract from the water.

Professor Pauly argues in a letter to TREE that there is a good reason why growth is not considered to be influenced by reproduction in the context of GOLT. While he agrees that reproductive output tends to scale hyperallometrically in fish, he does not agree that fish slow their growth because they allocate increasingly more to reproduction. Instead, he thinks that as growth slows (due to oxygen limitation caused by physical constraints on gill size) increased allocation of resources is directed to reproduction.

In their rebuttal, Dustin and Craig summarise their difference in opinion as one of causality; while Professor Pauly argues that body size in fish is limited by gill area, they believe that organs evolve to provide capacity to meet an organisms requirements. Or, in other words, the trait of body size is the product of selection whereby the size of an organisms is the best it can be to maximise fitness in a particular environment. Most importantly, taken to its logical extension, Dustin and Craig argue that Pauly’s own arguments imply fish reproduction should decrease with size.

In a separate letter, Michael Kearney from the University of Melbourne suggests that a radical revision of growth models is premature. In this case, Associate Professor Kearney suggests that a mechanistic modelling approach (such as Dynamic Energy Budget theory) based on a thermodynamically explicit theory of metabolism is better suited to understanding growth than the phenomenological modelling approach proposed by Dustin and Craig.

While Assoc. Prof. Kearney argues that the Dynamic Energy Budget model can incorporate hyperallometric scaling by adjusting the ‘rules’ governing how much energy is allocated to reproduction, Craig and Dustin say that to do this requires a phenomenological approach and is an unjustified post hoc model fitting solution. According to Craig and Dustin, this means that Assoc. Prof. Kearney’s model is not strictly mechanistic, with some parameters estimated by fitting mechanistic functions and some parameters requiring empirical data (a phenomenological approach).

But there is some agreement. Dustin, Craig and Michael Kearney are all interested in seeing studies of growth and metabolism that are conducted in the context of a full accounting of energy and mass balances (food in, changes in length and weight, respiration, faeces and eggs out) to continue improving our understanding of why organisms are the size they are.

You can read the original article and the follow-up letters.

Aquatic life history trajectories are shaped by selection, not oxygen limitation

Authors: Dustin J Marshall and Craig R White

Published in: Trends in Ecology & Evolution

Pauly1 argues that, as espoused in the gill-oxygen limitation theory (GOLT), growth slows as size increases because oxygen supply via the gills is unable to keep up with the oxygen demands of an increasingly large body. Thus, according to GOLT, growth determines the timing of reproduction, and fish reproduce when they become oxygen limited and growth starts to decline. GOLT has been critiqued on physiological grounds2,3 and we agree with those critiques. Large fish are no more oxygen limited than small fish, primarily because their respiratory surface area matches their metabolic demand for oxygen over a large size range…

Marshall DJ, White CR (2019) Aquatic life history trajectories are shaped by selection, not oxygen limitation, Trends in Ecology & Evolution. PDF DOI

Linking life-history theory and metabolic theory explains the offspring size-temperature relationship

Authors: Amanda K Pettersen, Craig R White, Robert J Bryson‐Richardson, and Dustin J Marshall

Published in: Ecology Letters

Abstract

Temperature often affects maternal investment in offspring. Across and within species, mothers in colder environments generally produce larger offspring than mothers in warmer environments, but the underlying drivers of this relationship remain unresolved.

We formally evaluated the ubiquity of the temperature–offspring size relationship and found strong support for a negative relationship across a wide variety of ectotherms. We then tested an explanation for this relationship that formally links life‐history and metabolic theories. We estimated the costs of development across temperatures using a series of laboratory experiments on model organisms, and a meta‐analysis across 72 species of ectotherms spanning five phyla.

We found that both metabolic and developmental rates increase with temperature, but developmental rate is more temperature sensitive than metabolic rate, such that the overall costs of development decrease with temperature. Hence, within a species’ natural temperature range, development at relatively cooler temperatures requires mothers to produce larger, better provisioned offspring.

Pettersen AK, White CR, Bryson-Richardson RJ, Marshall DJ (2019) Linking life-history theory and metabolic theory explains the offspring size-temperature relationship. Ecology Letters PDF DOI

Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

Authors: Colin Olito and Dustin J Marshall

Published in: Journal of Evolutionary Biology

Abstract

The idea that male reproductive strategies evolve primarily in response to sperm competition is almost axiomatic in evolutionary biology. However, externally fertilizing species, especially broadcast spawners, represent a large and taxonomically diverse group that have long challenged predictions from sperm competition theory – broadcast spawning males often release sperm slowly, with weak resource‐dependent allocation to ejaculates despite massive investment in gonads. One possible explanation for these counter‐intuitive patterns is that male broadcast spawners experience strong natural selection from the external environment during sperm dispersal.

Using a manipulative experiment, we examine how male reproductive success in the absence of sperm competition varies with ejaculate size and rate of sperm release, in the broadcast spawning marine invertebrate Galeolaria caespitosa (Polychaeta: Serpulidae).

We find that the benefits of Fast or Slow sperm release depend strongly on ejaculate size, but also that the per‐gamete fertilization rate decreases precipitously with ejaculate size.

Overall, these results suggest that, if males can facultatively adjust ejaculate size, they should slowly release small amounts of sperm. Recent theory for broadcast spawners predicts that sperm competition can also select for Slow release rates. Taken together, our results and theory suggest that selection often favours Slow ejaculate release rates whether males experience sperm competition or not.

Olito C, Marshall DJ (2018) Releasing small ejaculates slowly increases per‐gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae), Journal of Evolutionary Biology PDF DOI 

Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes

Authors: Tim Connallon, Shefali Sharma, and Colin Olito

Published in: The American Naturalist

The evolutionary trajectories of species with separate sexes depend on the effects of genetic variation on female and male traits as well as the direction and alignment of selection between the sexes.

Classical theory has shown that evolution is equally responsive to selection on females and males, with natural selection increasing the product of the average relative fitness of each sex over time.

This simple rule underlies several important predictions regarding the maintenance of genetic variation, the genetic basis of adaptation, and the dynamics of “sexually antagonistic” alleles. Nevertheless, theories of sex-specific selection overwhelmingly focus on evolution in constant environments, and it remains unclear whether they apply under changing conditions.

We derived four simple models of sex-specific selection in variable environments and explored how conditions of population subdivision, the timing of dispersal, sex differences in dispersal, and the nature of environmental change mediate the evolutionary dynamics of sex-specific adaptation.

We find that these dynamics are acutely sensitive to ecological, demographic, and life-history attributes that vary widely among species, with classical predictions breaking down in contexts of environmental heterogeneity.

The evolutionary rules governing sex-specific adaptation may therefore differ between species, suggesting new avenues for research on the evolution of sexual dimorphism.

Connallon T, Sharma S, Olito C (2018) Evolutionary consequences of sex-specific selection in variable environments: four simple models reveal diverse evolutionary outcomes, The American Naturalist PDF DOI

How does parental environment influence the potential for adaptation to global change?

Authors: Evatt Chirgwin, Dustin J Marshall, Carla M Sgrò, and Keyne Monro

Published in: Proceedings of the Royal Society B

Abstract

Parental environments are regularly shown to alter the mean fitness of offspring, but their impacts on the genetic variation for fitness, which predicts adaptive capacity and is also measured on offspring, are unclear. Consequently, how parental environments mediate adaptation to environmental stressors, like those accompanying global change, is largely unknown.

Here, using an ecologically important marine tubeworm in a quantitative-genetic breeding design, we tested how parental exposure to projected ocean warming alters the mean survival, and genetic variation for survival, of offspring during their most vulnerable life stage under current and projected temperatures.

Offspring survival was higher when parent and offspring temperatures matched. Across offspring temperatures, parental exposure to warming altered the distribution of additive genetic variance for survival, making it covary across current and projected temperatures in a way that may aid adaptation to future warming. Parental exposure to warming also amplified nonadditive genetic variance for survival, suggesting that compatibilities between parental genomes may grow increasingly important under future warming.

Our study shows that parental environments potentially have broader-ranging effects on adaptive capacity than currently appreciated, not only mitigating the negative impacts of global change but also reshaping the raw fuel for evolutionary responses to it.

Chirgwin E, Marshall DJ, Sgrò CM, Monro K (2018) How does parental environment influence the potential for adaptation to global change?, Proceedings of the Royal Society B PDF DOI

Global environmental drivers of marine fish egg size

Authors: Diego R Barneche, Scott C Burgess, and Dustin J Marshall

Published in: Global Ecology and Biogeography

Abstract

Aim: To test long‐standing theory on the role of environmental conditions (both mean and predictability) in shaping global patterns in the egg sizes of marine fishes.

Location: Global (50° S to 50° N).

Time period: 1880 to 2015.

Major taxa studied: Marine fish.

Methods: We compiled the largest geo‐located dataset of marine fish egg size (diameter) to date (n = 1,078 observations; 192 studies; 288 species; 242 localities). We decomposed sea surface temperature (SST) and chlorophyll‐a time series into mean and predictability (seasonality and colour of environmental noise – i.e. how predictable the environment is between consecutive time steps), and used these as predictors of egg size in a Bayesian phylogenetic hierarchical model. We test four specific hypotheses based on the classic discussion by Rass (1941), as well as contemporary life‐history theory, and the conceptual model of Winemiller and Rose (1992).

Results: Both environmental mean and predictability correlated with egg size. Our parsimonious model indicated that egg size decreases by c. 2.0‐fold moving from 1 to 30 °C. Environments that were more seasonal with respect to temperature were associated with larger eggs. Increasing mean chlorophyll‐a, from 0.1 to 1 mg/m3, was associated with a c. 1.3‐fold decrease in egg size. Lower chlorophyll‐a seasonality and reddened noise were also associated with larger egg sizes – aseasonal but more temporally autocorrelated resource regimes favoured larger eggs.

Main conclusions: Our findings support results from Rass (1941) and some predictions from Winemiller and Rose (1992). The effects of environmental means and predictability on marine fish egg size are largely consistent with those observed in marine invertebrates with feeding larvae, suggesting that there are important commonalities in how ectotherm egg size responds to environmental change. Our results further suggest that anthropogenically mediated changes in the environment will have profound effects on the distribution of marine life histories.

Barneche DR, Burgess SC, Marshall DJ (2018) Global environmental drivers of marine fish egg size, Global Ecology and Biogeography PDF DOI