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1.
PLoS Biol ; 21(5): e3002114, 2023 05.
Artigo em Inglês | MEDLINE | ID: mdl-37228036

RESUMO

Within many species, and particularly fish, fecundity does not scale with mass linearly; instead, it scales disproportionately. Disproportionate intraspecific size-reproduction relationships contradict most theories of biological growth and present challenges for the management of biological systems. Yet the drivers of reproductive scaling remain obscure and systematic predictors of how and why reproduction scaling varies are lacking. Here, we parameterise life history optimisation model to predict global patterns in the life histories of marine fishes. Our model predict latitudinal trends in life histories: Polar fish should reproduce at a later age and show steeper reproductive scaling than tropical fish. We tested and confirmed these predictions using a new, global dataset of marine fish life histories, demonstrating that the risks of mortality shape maturation and reproductive scaling. Our model also predicts that global warming will profoundly reshape fish life histories, favouring earlier reproduction, smaller body sizes, and lower mass-specific reproductive outputs, with worrying consequences for population persistence.


Assuntos
Peixes , Reprodução , Animais , Peixes/fisiologia , Fertilidade , Aquecimento Global
2.
Proc Natl Acad Sci U S A ; 119(21): e2200713119, 2022 05 24.
Artigo em Inglês | MEDLINE | ID: mdl-35594402

RESUMO

Body size covaries with population dynamics across life's domains. Metabolism may impose fundamental constraints on the coevolution of size and demography, but experimental tests of the causal links remain elusive. We leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Over the course of their evolution, the cells have roughly doubled in size relative to their ancestors. These larger cells have metabolic rates that are absolutely higher, but relative to their size, they are lower. Metabolic theory successfully predicted the relations between size, metabolism, and maximum population density, including support for Damuth's law of energy equivalence, such that populations of larger cells achieved lower maximum densities but higher maximum biomasses than populations of smaller cells. The scaling of metabolism with cell size thus predicted the scaling of size with maximum population density. In stark contrast to standard theory, however, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental and intuitive assumption that the costs of building new individuals should scale directly with their size. The finding that the costs of production can be decoupled from size necessitates a reevaluation of the evolutionary drivers and ecological consequences of biological size more generally.


Assuntos
Ecologia , Escherichia coli , Evolução Biológica , Escherichia coli/genética , Escherichia coli/metabolismo
3.
Physiology (Bethesda) ; 38(6): 0, 2023 11 01.
Artigo em Inglês | MEDLINE | ID: mdl-37698354

RESUMO

Most explanations for the relationship between body size and metabolism invoke physical constraints; such explanations are evolutionarily inert, limiting their predictive capacity. Contemporary approaches to metabolic rate and life history lack the pluralism of foundational work. Here, we call for reforging of the lost links between optimization approaches and physiology.


Assuntos
Metabolismo Energético , Modelos Biológicos , Humanos , Tamanho Corporal/fisiologia , Metabolismo Energético/fisiologia
4.
Ecol Lett ; 27(4): e14400, 2024 Apr.
Artigo em Inglês | MEDLINE | ID: mdl-38591235

RESUMO

Good experimental design is critical for sound empirical ecology and evolution. However, many contemporary studies fail to replicate at the appropriate biological or organizational level, so causal inference might have less vigorous support than often assumed. Here, I provide a guide for how to identify the appropriate scale of replication for a range of common experimental designs in ecological and evolutionary studies. I discuss the merits of replicating multiple scales of biological organization. I suggest that experimental design be discussed in terms of the scale of replication relative to the scale at which inferences are sought when designing, discussing and reviewing experiments in ecology and evolution. I also suggest that more conversations about experimental design are needed, and I hope this piece stimulates such conversation.


Assuntos
Ecologia , Projetos de Pesquisa , Evolução Biológica
5.
J Exp Biol ; 227(6)2024 Mar 15.
Artigo em Inglês | MEDLINE | ID: mdl-38380562

RESUMO

From bacteria to metazoans, higher density populations have lower per capita metabolic rates than lower density populations. The negative covariance between population density and metabolic rate is thought to represent a form of adaptive metabolic plasticity. A relationship between density and metabolism was actually first noted 100 years ago, and was focused on spermatozoa; even then, it was postulated that adaptive plasticity drove this pattern. Since then, contemporary studies of sperm metabolism specifically assume that sperm concentration has no effect on metabolism and that sperm metabolic rates show no adaptive plasticity. We did a systematic review to estimate the relationship between sperm aerobic metabolism and sperm concentration, for 198 estimates spanning 49 species, from protostomes to humans from 88 studies. We found strong evidence that per capita metabolic rates are concentration dependent: both within and among species, sperm have lower metabolisms in dense ejaculates, but increase their metabolism when diluted. On average, a 10-fold decrease in sperm concentration increased per capita metabolic rate by 35%. Metabolic plasticity in sperm appears to be an adaptive response, whereby sperm maximize their chances of encountering eggs.

6.
Proc Natl Acad Sci U S A ; 118(34)2021 08 24.
Artigo em Inglês | MEDLINE | ID: mdl-34417293

RESUMO

Metabolism should drive demography by determining the rates of both biological work and resource demand. Long-standing "rules" for how metabolism should covary with demography permeate biology, from predicting the impacts of climate change to managing fisheries. Evidence for these rules is almost exclusively indirect and in the form of among-species comparisons, while direct evidence is exceptionally rare. In a manipulative field experiment on a sessile marine invertebrate, we created experimental populations that varied in population size (density) and metabolic rate, but not body size. We then tested key theoretical predictions regarding relationships between metabolism and demography by parameterizing population models with lifetime performance data from our field experiment. We found that populations with higher metabolisms had greater intrinsic rates of increase and lower carrying capacities, in qualitative accordance with classic theory. We also found important departures from theory-in particular, carrying capacity declined less steeply than predicted, such that energy use at equilibrium increased with metabolic rate, violating the long-standing axiom of energy equivalence. Theory holds that energy equivalence emerges because resource supply is assumed to be independent of metabolic rate. We find this assumption to be violated under real-world conditions, with potentially far-reaching consequences for the management of biological systems.


Assuntos
Metabolismo Basal , Briozoários/fisiologia , Conservação dos Recursos Naturais , Ecossistema , Metabolismo Energético , Modelos Biológicos , Migração Animal , Animais , Demografia , Densidade Demográfica
7.
Proc Natl Acad Sci U S A ; 118(34)2021 08 24.
Artigo em Inglês | MEDLINE | ID: mdl-34400498

RESUMO

Marine fisheries are an essential component of global food security, but many are close to their limits and some are overfished. The models that guide the management of these fisheries almost always assume reproduction is proportional to mass (isometry), when fecundity generally increases disproportionately to mass (hyperallometry). Judged against several management reference points, we show that assuming isometry overestimates the replenishment potential of exploited fish stocks by 22% (range: 2% to 78%) for 32 of the world's largest fisheries, risking systematic overharvesting. We calculate that target catches based on assumptions of isometry are more than double those based on assumptions of hyperallometry for most species, such that common reference points are set twice as high as they should be to maintain the target level of replenishment. We also show that hyperallometric reproduction provides opportunities for increasing the efficacy of tools that are underused in standard fisheries management, such as protected areas or harvest slot limits. Adopting management strategies that conserve large, hyperfecund fish may, in some instances, result in higher yields relative to traditional approaches. We recommend that future assessment of reference points and quotas include reproductive hyperallometry unless there is clear evidence that it does not occur in that species.


Assuntos
Pesqueiros/organização & administração , Peixes/fisiologia , Reprodução/fisiologia , Animais , Conservação dos Recursos Naturais , Peixes/classificação , Dinâmica Populacional , Especificidade da Espécie
8.
Am Nat ; 202(4): 448-457, 2023 10.
Artigo em Inglês | MEDLINE | ID: mdl-37792921

RESUMO

AbstractThe evolution of internal fertilization has occurred repeatedly and independently across the tree of life. As it has evolved, internal fertilization has reshaped sexual selection and the covariances among sexual traits, such as testes size, and gamete traits. But it is unclear whether fertilization mode also shows evolutionary associations with traits other than primary sex traits. Theory predicts that fertilization mode and body size should covary, but formal tests with phylogenetic control are lacking. We used a phylogenetically controlled approach to test the covariance between fertilization mode and adult body size (while accounting for latitude, offspring size, and offspring developmental mode) among 1,232 species of marine invertebrates from three phyla. Within all phyla, external fertilizers are consistently larger than internal fertilizers: the consequences of fertilization mode extend to traits that are only indirectly related to reproduction. We suspect that other traits may also coevolve with fertilization mode in ways that remain unexplored.


Assuntos
Evolução Biológica , Fertilização , Filogenia , Fertilizantes , Reprodução , Tamanho Corporal
9.
J Exp Biol ; 226(11)2023 06 01.
Artigo em Inglês | MEDLINE | ID: mdl-37249068

RESUMO

Constraint-based explanations have dominated theories of size-related patterns in nature for centuries. Explanations for metabolic scaling - the way in which metabolism changes with body mass - have been based on the geometry of circulatory networks through which resources are distributed, the need to dissipate heat produced as a by-product of metabolic processes, and surface-area-to-volume constraints on the flux of nutrients or waste. As an alternative to these constraint-based approaches, we recently developed a new theory that predicts that metabolic allometry arises as a consequence of the optimisation of growth and reproduction to maximise fitness within a finite life. Our theory is free of physical geometric constraints that limit the possibilities available to evolution, and we therefore argue that metabolic allometry can be explained without the need to invoke any of the assumed constraints traditionally imposed by metabolic theories. Our findings also suggest that metabolism, growth and reproduction have co-evolved to maximise fitness (i.e. lifetime reproduction) and that the observed patterns in these fundamental characteristics of life can similarly be explained by optimisation rather than constraint. In this Centenary Commentary, we present an overview of our approach and a critique of its limitations. We propose a suite of empirical tests that we hope will move the field forward, discuss the dangers of model overparameterisation and highlight the need to remain open to non-adaptive hypotheses for the origin of biological patterns.


Assuntos
Metabolismo Energético , Reprodução , Modelos Biológicos , Biologia
10.
Glob Chang Biol ; 28(2): 390-402, 2022 01.
Artigo em Inglês | MEDLINE | ID: mdl-34674354

RESUMO

The distribution of disease vectors such as mosquitoes is changing. Climate change, invasions and vector control strategies all alter the distribution and abundance of mosquitoes. When disease vectors undergo a range shift, so do disease burdens. Predicting such shifts is a priority to adequately prepare for disease control. Accurate predictions of distributional changes depend on how factors such as temperature and competition affect mosquito life-history traits, particularly body size and reproduction. Direct estimates of both body size and reproduction in mosquitoes are logistically challenging and time-consuming, so the field has long relied upon linear (isometric) conversions between wing length (a convenient proxy of size) and reproductive output. These linear transformations underlie most models projecting species' distributions and competitive interactions between native and invasive disease vectors. Using a series of meta-analyses, we show that the relationship between wing length and fecundity are nonlinear (hyperallometric) for most mosquito species. We show that whilst most models ignore reproductive hyperallometry (with respect to wing length), doing so introduces systematic biases into estimates of population growth. In particular, failing to account for reproductive hyperallometry overestimates the effects of temperature and underestimates the effects of competition. Assuming isometry also increases the potential to misestimate the efficacy of vector control strategies by underestimating the contribution of larger females in population replenishment. Finally, failing to account for reproductive hyperallometry and variation in body size can lead to qualitative errors via the counter-intuitive effects of Jensen's inequality. For example, if mean sizes decrease, but variance increases, then reproductive outputs may actually increase. We suggest that future disease vector models incorporate hyperallometric relationships to more accurately predict changes in mosquito distribution in response to global change.


Assuntos
Vetores de Doenças , Reprodução , Animais , Tamanho Corporal , Mudança Climática , Feminino , Fertilidade
11.
Am Nat ; 197(4): 448-460, 2021 04.
Artigo em Inglês | MEDLINE | ID: mdl-33755536

RESUMO

AbstractMultilevel selection on offspring size occurs when offspring fitness depends on both absolute size (hard selection) and size relative to neighbors (soft selection). We examined multilevel selection on egg size at two biological scales-within clutches and among clutches from different females-using an external fertilizing tube worm. We exposed clutches of eggs to two sperm environments (limiting and saturating) and measured their fertilization success. We then modeled environmental (sperm-dependent) differences in hard and soft selection on individual eggs as well as selection on clutch-level traits (means and variances). Hard and soft selection differed in strength and form depending on sperm availability-hard selection was consistently stabilizing; soft selection was directional and favored eggs relatively larger (sperm limitation) or smaller (sperm saturation) than the clutch mean. At the clutch level, selection on mean egg size was largely concave, while selection on within-clutch variance was weak but generally negative-although some correlational selection occurred between these two traits. Importantly, we found that the optimal clutch mean egg size differed for mothers and offspring, suggesting some antagonism between the levels of selection. We thus identify several pathways that may maintain offspring size variation: environmentally (sperm-) dependent soft selection, antagonistic multilevel selection, and correlational selection on clutch means and variances. Multilevel approaches are powerful but seldom-used tools for studies of offspring size, and we encourage their future use.


Assuntos
Fertilização , Modelos Genéticos , Óvulo , Poliquetos/genética , Seleção Genética , Animais , Tamanho da Ninhada , Feminino , Masculino
12.
New Phytol ; 229(5): 2647-2659, 2021 03.
Artigo em Inglês | MEDLINE | ID: mdl-33156533

RESUMO

Cell size influences the rate at which phytoplankton assimilate dissolved inorganic carbon (DIC), but it is unclear whether volume-specific carbon uptake should be greater in smaller or larger cells. On the one hand, Fick's Law predicts smaller cells to have a superior diffusive CO2 supply. On the other, larger cells may have greater scope to invest metabolic energy to upregulate active transport per unit area through CO2 -concentrating mechanisms (CCMs). Previous studies have focused on among-species comparisons, which complicates disentangling the role of cell size from other covarying traits. In this study, we investigated the DIC assimilation of the green alga Dunaliella tertiolecta after using artificial selection to evolve a 9.3-fold difference in cell volume. We compared CO2 affinity, external carbonic anhydrase (CAext ), isotopic signatures (δ13 C) and growth among size-selected lineages. Evolving cells to larger sizes led to an upregulation of CCMs that improved the DIC uptake of this species, with higher CO2 affinity, higher CAext and higher δ13 C. Larger cells also achieved faster growth and higher maximum biovolume densities. We showed that evolutionary shifts in cell size can alter the efficiency of DIC uptake systems to influence the fitness of a phytoplankton species.


Assuntos
Anidrases Carbônicas , Fitoplâncton , Carbono , Dióxido de Carbono , Anidrases Carbônicas/metabolismo , Tamanho Celular , Fotossíntese , Fitoplâncton/metabolismo
13.
Proc Biol Sci ; 287(1933): 20200995, 2020 08 26.
Artigo em Inglês | MEDLINE | ID: mdl-32811317

RESUMO

Size and metabolism are highly correlated, so that community energy flux might be predicted from size distributions alone. However, the accuracy of predictions based on interspecific energy-size relationships relative to approaches not based on size distributions is unknown. We compare six approaches to predict energy flux in phytoplankton communities across succession: assuming a constant energy use among species (per cell or unit biomass), using energy-size interspecific scaling relationships and species-specific rates (both with or without accounting for density effects). Except for the per cell approach, all others explained some variation in energy flux but their accuracy varied considerably. Surprisingly, the best approach overall was based on mean biomass-specific rates, followed by the most complex (species-specific rates with density). We show that biomass-specific rates alone predict community energy flux because the allometric scaling of energy use with size measured for species in isolation does not reflect the isometric scaling of these species in communities. We also find energy equivalence throughout succession, even when communities are not at carrying capacity. Finally, we discuss that species assembly can alter energy-size relationships, and that metabolic suppression in response to density might drive the allometry of community energy flux as biomass accumulates.


Assuntos
Ecossistema , Fitoplâncton , Biomassa , Tamanho Corporal , Metabolismo Energético , Modelos Biológicos , Densidade Demográfica
14.
J Exp Biol ; 223(Pt 17)2020 09 04.
Artigo em Inglês | MEDLINE | ID: mdl-32709627

RESUMO

Within species, individuals of the same size can vary substantially in their metabolic rate. One source of variation in metabolism is conspecific density - individuals in denser populations may have lower metabolism than those in sparser populations. However, the mechanisms through which conspecifics drive metabolic suppression remain unclear. Although food competition is a potential driver, other density-mediated factors could act independently or in combination to drive metabolic suppression, but these drivers have rarely been investigated. We used sessile marine invertebrates to test how food availability interacts with oxygen availability, water flow and chemical cues to affect metabolism. We show that conspecific chemical cues induce metabolic suppression independently of food and this metabolic reduction is associated with the downregulation of physiological processes rather than feeding activity. Conspecific cues should be considered when predicting metabolic variation and competitive outcomes as they are an important, but underexplored, source of variation in metabolic traits.


Assuntos
Sinais (Psicologia) , Humanos
15.
Ecol Lett ; 22(11): 1879-1888, 2019 Nov.
Artigo em Inglês | MEDLINE | ID: mdl-31468661

RESUMO

Species simultaneously compete with and facilitate one another. Size can mediate transitions along this competition-facilitation continuum, but the consequences for demography are unclear. We orthogonally manipulated the size of a focal species, and the size and density of a heterospecific neighbour, in the field using a model marine system. We then parameterised a size-structured population model with our experimental data. We found that heterospecific size and density interactively altered the population dynamics of the focal species. Size determined whether heterospecifics facilitated (when small) or competed with (when large) the focal species, while density strengthened these interactions. Such size-mediated interactions also altered the pace of the focal's life history. We provide the first demonstration that size and density mediate competition and facilitation from a population dynamical perspective. We suspect such effects are ubiquitous, but currently underappreciated. We reiterate classic cautions against inferences about competitive hierarchies made in the absence of size-specific data.


Assuntos
Modelos Biológicos , Densidade Demográfica , Dinâmica Populacional
16.
Ecol Lett ; 22(9): 1407-1416, 2019 Sep.
Artigo em Inglês | MEDLINE | ID: mdl-31206970

RESUMO

Body size often strongly covaries with demography across species. Metabolism has long been invoked as the driver of these patterns, but tests of causal links between size, metabolism and demography within a species are exceedingly rare. We used 400 generations of artificial selection to evolve a 2427% size difference in the microalga Dunaliella tertiolecta. We repeatedly measured size, energy fluxes and demography across the evolved lineages. Then, we used standard metabolic theory to generate predictions of how size and demography should covary based on the scaling of energy fluxes that we measured. The size dependency of energy remained relatively consistent in time, but metabolic theory failed to predict demographic rates, which varied unpredictably in strength and even sign across generations. Classic theory holds that size affects demography via metabolism - our results suggest that both metabolism and size act separately to drive demography and that among-species patterns may not predict within-species processes.


Assuntos
Tamanho Celular , Clorofíceas/metabolismo , Metabolismo Energético , Modelos Biológicos , Biomassa , Clorofíceas/citologia , Densidade Demográfica
17.
Ecol Lett ; 22(3): 518-526, 2019 Mar.
Artigo em Inglês | MEDLINE | ID: mdl-30618178

RESUMO

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.


Assuntos
Tamanho Corporal , Mães , Temperatura , Adaptação Fisiológica , Animais , Feminino
18.
J Evol Biol ; 32(2): 177-186, 2019 02.
Artigo em Inglês | MEDLINE | ID: mdl-30461107

RESUMO

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.


Assuntos
Fertilização , Poliquetos/fisiologia , Animais , Evolução Biológica , Ejaculação , Masculino , Seleção Genética
19.
Ecol Lett ; 21(1): 54-62, 2018 Jan.
Artigo em Inglês | MEDLINE | ID: mdl-29143436

RESUMO

Size imposes physiological and ecological constraints upon all organisms. Theory abounds on how energy flux covaries with body size, yet causal links are often elusive. As a more direct way to assess the role of size, we used artificial selection to evolve the phytoplankton species Dunaliella tertiolecta towards smaller and larger body sizes. Within 100 generations (c. 1 year), we generated a fourfold difference in cell volume among selected lineages. Large-selected populations produced four times the energy than small-selected populations of equivalent total biovolume, but at the cost of much higher volume-specific respiration. These differences in energy utilisation between large (more productive) and small (more energy-efficient) individuals were used to successfully predict ecological performance (r and K) across novel resource regimes. We show that body size determines the performance of a species by mediating its net energy flux, with worrying implications for current trends in size reduction and for global carbon cycles.


Assuntos
Evolução Biológica , Tamanho Corporal , Tamanho Celular , Ecologia , Fitoplâncton
20.
Ecol Lett ; 21(8): 1182-1190, 2018 08.
Artigo em Inglês | MEDLINE | ID: mdl-29781121

RESUMO

Robert MacArthur developed a theory of community assembly based on competition. By incorporating energy flow, MacArthur's theory allows for predictions of community function. A key prediction is that communities minimise energy wastage over time, but this minimisation is a trade-off between two conflicting processes: exploiting food resources, and maintaining low metabolism and mortality. Despite its simplicity and elegance, MacArthur's principle has not been tested empirically despite having long fascinated theoreticians. We used a combination of field chronosequence experiments and laboratory assays to estimate how the energy wastage of a community changes during succession. We found that older successional stages wasted more energy in maintenance, but there was no clear pattern in how communities of different age exploited food resources. We identify several reasons for why MacArthur's original theory may need modification and new avenues to further explore community efficiency, an understudied component of ecosystem functioning.


Assuntos
Ecossistema , Modelos Teóricos
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