Biol. Rev. (2014), 89, pp. 849–859. 849 doi: 10.1111/brv.12082 Resource allocation to reproduction in animals Sebastiaan A. L. M. Kooijman1,∗ and Konstadia Lika2 1Department of Theoretical Biology, VU University Amsterdam, de Boelelaan 1087, 1081 HV Amsterdam, The Netherlands 2Department of Biology, University of Crete, Voutes University Campus, 70013 Heraklion, Crete, Greece ABSTRACT The standard Dynamic Energy Budget (DEB) model assumes that a fraction κ of mobilised reserve is allocated to somatic maintenance plus growth, while the rest is allocated to maturity maintenance plus maturation (in embryos and juveniles) or reproduction (in adults). All DEB parameters have been estimated for 276 animal species from most large phyla and all chordate classes. The goodness of fit is generally excellent. We compared the estimated values of κ with those that would maximise reproduction in fully grown adults with abundant food. Only 13% of these species show a reproduction rate close to the maximum possible (assuming that κ can be controlled), another 4% have κ lower than the optimal value, and 83% have κ higher than the optimal value. Strong empirical support hence exists for the conclusion that reproduction is generally not maximised. We also compared the parameters of the wild chicken with those of races selected for meat and egg production and found that the latter indeed maximise reproduction in terms of κ, while surface-specific assimilation was not affected by selection. We suggest that small values of κ relate to the down-regulation of maximum body size, and large values to the down-regulation of reproduction. We briefly discuss the ecological context for these findings. Key words: animal reproduction, dynamic energy budget, allocation to soma, chicken egg production, selection. CONTENTS I. Introduction ................................................................................................ 849 II. Materials and methods ..................................................................................... 850 III. Sub- and supra-optimality .................................................................................. 851 IV. Selection for maximum reproduction ...................................................................... 853 V. Discussion .................................................................................................. 854 VI. Conclusions ................................................................................................ 857 VII. Acknowledgements ......................................................................................... 857 VIII. References .................................................................................................. 857 IX. Appendix ................................................................................................... 858 X. The standard deb model with acceleration ................................................................. 858 I. INTRODUCTION Herein we aim to quantify resource allocation to reproduction in animals within the context of DEB theory. Investment in reproduction is subject to intense ecological One of the parameters of the standard DEB model is of and evolutionary debate (Roff, 1992; Stearns, 1992; Flatt & particular interest here: the fraction κ of mobilised reserve Heyland, 2011). Some species have many small offspring, that is allocated to soma (somatic maintenance plus growth), others a few large ones, but we are unaware of a broad as opposed to maturity maintenance plus reproduction. All comparative study of relative investment in reproduction parameters of the standard DEB model have now been compared to growth. This is probably because a single estimated for 276 species, see the add my pet collection metabolic framework is required that applies to all species for at http://www.bio.vu.nl/thb/deb/deblab/add_my_pet/ their full life cycle (including embryo development). Dynamic Species.html. We evaluated the reproduction rate of a fully Energy Budget (DEB) theory offers such a framework for grown female with abundant food for each species and metabolic organisation (Kooijman, 2010). compared it with the value assuming an optimal value of κ, * Address for correspondence (Tel: +31 20 5987130; E-mail: [email protected]). Biological Reviews 89 (2014) 849–859 © 2014 The Authors. Biological Reviews © 2014 Cambridge Philosophical Society 850 Sebastiaan A. L. M. Kooijman and Konstadia Lika here defined as the value that maximises reproduction rate. organisation is discussed in Lika & Kooijman (2011). The At an early stage of the formation of this large collection mobilisation rate is such that weak homeostasis is preserved: we reported that most animal species in the collection reserve density, i.e. the ratio of the amounts of reserve invest remarkably little in reproduction (Lika, Kearney and structure, does not change during growth after birth & Kooijman, 2011b). Now, with five times more species as long as food density remains constant. A fraction κ available, we reconsider this observation and report on a of this mobilised flux is allocated to somatic maintenance case-study with different races of chickens, the wild race, and growth (soma), the rest to maturity maintenance and one selected for meat production and one selected for egg maturation (in embryos and juveniles) or reproduction (in production. Selection can be shown to have affected some adults). Food intake is proportional to surface area, which is parameters in a remarkable way. proportional to volume to the 2/3 power in isomorphs, but embryos do not eat. Somatic maintenance is proportional to the amount of structure, maturity maintenance to the II. MATERIALS AND METHODS level of maturity. Maturity has no mass or energy and is quantified as cumulative investment of reserve. Feeding and allocation to reproduction are initiated if maturity reaches The data collection does not consist of randomly chosen threshold values. Allocation to reproduction is accumulated species. Indeed, a randomly chosen sample of all species would consist largely of insects, probably mostly beetles, in a reproduction buffer; the rules for converting this buffer and data on these species are few. The number of extant to eggs are species specific. Investment in an egg is such that undescribed animal species is unknown, but may be large reserve density of the neonate equals that of the mother at relative to the described species. Thus, data availability egg laying (known as the maternal effect). Apart from rules is a serious problem that constrains the choice of species, for food searching and ageing, these few criteria fully specify although we tried to include as many phyla as possible. Apart the standard DEB model. Biomass is, therefore, assumed from sponges, nemerteans and nematomorphs, all phyla to consist of reserve, structure and, possibly, a reproduction with more than 400 species are included, incorporating buffer; these types are treated as (formal) pools of metabolites 13 chordate classes, and all bird and mammal orders each with constant composition. (apart from marsupial moles). The collection spans a Application to a large number of animal species revealed body size range from 10−8 to 108 g, from hairy back that many species accelerate their metabolism after birth Aspidiophorus polystictos to blue whale Balaenoptera musculus. (Kooijman et al., 2011). This can be captured realistically as It includes over 100 different data types on all aspects a simple extension of the standard DEB model by assuming of energetics (growth, reproduction, respiration, product that these species deviate from isomorphy during their early formation, feeding) and all life stages (embryo, juvenile, juvenile phase, where surface area is (temporarily) propor- adult), collected in a collaborative effort involving more tional to volume, rather than to volume to the 2/3 power. than 60 researchers. The parameters of the standard DEB Acceleration affects both specific assimilation and energy model have been estimated using the covariation method conductance, which is why acceleration is of importance to (Lika et al., 2011a) and the software package DEBtool allocation to reproduction. Surface-area-specific assimilation (http://www.bio.vu.nl/thb/deb/deblab/debtool/). The increases during ontogeny and fuels reproduction, and mean goodness of fit is very high, 8.3 on a scale from energy conductance controls reserve mobilisation, so -∞to10, but the mean completeness level of the data is dominates developmental rate and cumulative maintenance low, 2.5 on a scale from 0 to 10; see Lika et al. (2011a)for costs until birth, when feeding starts. This affects the cost criteria. The data, as extracted from the literature, are given per offspring. with references, the species-specific code, the predictions for The most essential feature of the standard DEB model the data that we obtained, the resulting parameter values in the present context is that the energy cost for a and a list of over 100 implied properties can be inspected neonate follows from the cost for structure, maturation for each species. All of this can be found at the website and maintenance, in combination with size at birth. This of the collection (information about the DEB research involves parameters that can be estimated from data on program is available at: http://www.bio.vu.nl/thb/deb/; post-embryonic development; embryo data are available the add my pet collection is available at http://www.bio. for a few species only. To our knowledge, the standard