Substantial intraspecific variation in energy budgets: Biology or artefact?

Tomos Potter,David N Reznick,Tim Coulson

doi:10.1111/1365-2435.13847

Tomos Potter, David N Reznick + Show 1 more

Open Access

https://doi.org/10.1111/1365-2435.13847

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Abstract

Abstract Dynamic energy budget (DEB) theory provides a model of the intrinsic energetic trade‐offs that shape life histories, in terms of fluxes of energy through biological processes. In these models, life histories are a function of environmental conditions and of fundamental traits of the organism relating to the acquisition, allocation and use of energy. These traits are described by the parameters of the DEB model, which are typically estimated from multiple data sources. DEB parameters have been estimated for over 2,500 species, and recent work has aimed to compare species on the basis of differences in parameter values. However, little is known about intraspecific variation in DEB parameters, and the reliability of comparisons between parameter sets is rarely tested. We estimated DEB parameters for 16 populations of Trinidadian guppy. Our objectives were to determine whether DEB theory could characterise known life‐history differences between populations, and to assess whether differences in parameter values between populations were reliable indicators of biological differences. We found substantial intraspecific variation in parameter values. The models accurately reproduced biological processes, and also predicted differences in resource allocation and metabolic rate consistent with known life‐history differences among these populations. However, parameter estimates varied substantially as an artefact of the amount and types of data used to fit the models. This bias appeared to be systematic, influencing estimates for multiple populations in a comparable fashion. We show that similar patterns of growth and reproduction can be reproduced with very different parameter sets. Our results imply that comparisons of DEB parameters between models fit with different types of data may reflect artefactual rather than biological differences. A free Plain Language Summary can be found within the Supporting Information of this article.

Highlights

The variety of life-history strategies observed in the natural world is truly astounding
Guppy ecotypes adapted to high- and low-predation-risk environments differ in how they obtain, allocate and use resources: we found that Dynamic energy budget (DEB) parameters differed between ecotype pairs, and that these differences were often consistent between independent evolutionary origins of ecotype pairs in the Oropuche river and Yarra rivers. (Table 4, Figure 3)
Our objectives in this study centred around two questions: (1) Can DEB theory characterise well-known life-history variation among populations of the Trinidadian guppy? and (2) Do parameterised DEB models reliably describe energy budgets such that populations and species can be compared by the difference in their parameter values? The answer to the first question is ‘yes’, in that DEB models reproduced population-specific patterns of growth, development and reproduction, and qualitatively predicted known differences between guppy ecotypes in resource allocation and metabolic rate

Summary

Introduction

The variety of life-history strategies observed in the natural world is truly astounding. Classical theory proposes that life-history evolution is driven by the interaction between (a) extrinsic ecological effects on reproduction and survival and (b) intrinsic organismal constraints, arising from trade-offs in the allocation of energy to different biological processes (Stearns, 1989, 2000). Detection of these intrinsic energetic trade-offs has been successful across taxa (Bauwens & Díaz-Uriarte, 1997; Healy et al, 2019; Salguero-Gómez et al, 2016; Stearns, 1983), but less so within species (van Noordwijk & de Jong, 1986). For a mechanistic understanding of life-history evolution, a model that captures the intrinsic trade-o ffs involved in developing and expressing traits that underpin the acquisition, allocation and use of resources is required

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