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The Conversation: ‘Let’s get real’: scientists discover a new way climate change threatens cold-blooded animals

This article is republished from The Conversation under a Creative Commons license. Read the original article.

All animals need energy to live. They use it to breathe, circulate blood, digest food and move. Young animals use energy to grow, and later in life, to reproduce.

Increased body temperature increases the rate at which an animal uses energy. Because cold-blooded animals rely on the thermal conditions of their environment to regulate their body temperature, they’re expected to need more energy as the planet warms.

However, our new research, published today in Nature Climate Change, suggests temperature is not the only environmental factor affecting the future energy needs of cold-blooded animals. How they interact with other species will also play a role.

Our findings suggest cold-blooded animals will need even more energy in a warmer world than previously thought. This may increase their extinction risk.

Young animals use energy to grow, and later in life, to reproduce.

What we already know

The amount of energy animals use in a given amount of time is called their metabolic rate.

Metabolic rate is influenced by a variety of factors, including body size and activity levels. Larger animals have higher metabolic rates than smaller animals, and active animals have higher metabolic rates than inactive animals.

Metabolic rate also depends on body temperature. This is because temperature affects the rate at which the biochemical reactions involved in energy metabolism proceed. Generally, if an animal’s body temperature increases, its metabolic rate will accelerate exponentially.

Most animals alive today are cold-blooded, or “ectotherms”. Insects, worms, fish, crustaceans, amphibians and reptiles – basically all creatures except mammals and birds – are ectotherms.

As human-induced climate change raises global temperatures, the body temperatures of cold-blooded animals are also expected to rise.

Researchers say the metabolic rate of some land-based ectotherms may have already increased by between 3.5% and 12% due to climate warming that’s already occurred. But this prediction doesn’t account for the animals’ capacity to physiologically “acclimate” to warmer temperatures.

Acclimation refers to an animal’s ability to remodel its physiology to cope with a change in its environment.

But rarely can acclimation fully negate the effect of temperature on metabolic processes. For this reason, by the end of the century land-based ectotherms are still predicted to have metabolic rates about 20% to 30% higher than they are now.

Having a higher metabolic rate means that animals will need more food. This means they might starve if more food is not available, and leaves them less energy to find a mate and reproduce.

As climate change raises global temperatures, the body temperatures of cold-blooded animals are also expected to rise.

Our research

Previous research attempts to understand the energetic costs of climate warming for ectotherms were limited in one important respect. They predominantly used animals studied in relatively simple laboratory environments where the only challenge they faced was a change in temperature.

However, animals face many other challenges in nature. This includes interacting with other species, such as competing for food and predator-prey relationships.

Even though species interact all the time in nature, we rarely study how this affects metabolic rates.

We wanted to examine how species interactions might alter predictions about the energetic costs of climate warming for cold-blooded animals. To do this, we turned to the fruit fly (from the genus Drosophila).

Fruit fly species lay their eggs in rotting plant material. The larvae that hatch from these eggs interact and compete for food.

Our study involved rearing fruit fly species alone or together at different temperatures. We found when two species of fruit fly larvae compete for food at warmer temperatures, they were more active as adults than adults that didn’t compete with other species as larvae. This means they also used more energy.

From this, we used modelling to deduce that species interactions at warmer global temperatures increase the future energy needs of fruit flies by between 3% and 16%.

These findings suggest previous studies have underestimated the energetic cost of climate warming for ectotherms. That means purely physiological approaches to understanding the consequences of climate change for cold-blooded animals are likely to be insufficient.

Previous studies have underestimated the energetic cost of climate warming for ectotherms.

Let’s get real

Understanding the energy needs of animals is important for understanding how they’ll survive, reproduce and evolve in challenging environments.

In a warmer world, hotter ectotherms will need more energy to survive and reproduce. If there is not enough food to meet their bodies’ energy demands, their extinction risk may increase.

Clearly, we must more accurately predict how climate warming will threaten biodiversity. This means studying the responses of animals to temperature change under more realistic conditions.
The Conversation

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Interspecific interactions alter the metabolic costs of climate warming

Authors: Lesley A Alton and Vanessa Kellermann

Published in: Nature Climate Change

Abstract

Climate warming is expected to increase the energy demands of ectotherms by accelerating their metabolic rates exponentially. However, this prediction ignores environmental complexity such as species interactions.

Here, to better understand the metabolic costs of climate change for ectotherms, we reared three Drosophila species in either single-species or two-species cultures at different temperatures and projected adult metabolic responses under an intermediate climate-warming scenario across the global range of Drosophila.

We determined that developmental acclimation to warmer temperatures can reduce the energetic cost of climate warming from 39% to ~16% on average by reducing the thermal sensitivity of metabolic rates. However, interspecific interactions among larvae can erode this benefit of developmental thermal acclimation by increasing the activity of adults that develop at warmer temperatures.

Thus, by ignoring species interactions we risk underestimating the metabolic costs of warming by 3–16% on average.

Alton LA, Kellermann V (2023) Interspecific interactions alter the metabolic costs of climate warming. Nature Climate Change DOI

dustinmeeg

Mapping the correlations and gaps in studies of complex life histories

Authors: Emily L Richardson and Dustin J Marshall

Published in: Ecology and Evolution

Abstract

For species with complex life histories, phenotypic correlations between life-history stages constrain both ecological and evolutionary trajectories.

Studies that seek to understand correlations across the life history differ greatly in their experimental approach: some follow individuals (“individual longitudinal”), while others follow cohorts (“cohort longitudinal”). Cohort longitudinal studies risk confounding results through Simpson’s Paradox, where correlations observed at the cohort level do not match that of the individual level. Individual longitudinal studies are laborious in comparison, but provide a more reliable test of correlations across life-history stages.

Our understanding of the prevalence, strength, and direction of phenotypic correlations depends on the approaches that we use, but the relative representation of different approaches remains unknown.

Using marine invertebrates as a model group, we used a formal, systematic literature map to screen 17,000+ papers studying complex life histories, and characterized the study type (i.e., cohort longitudinal, individual longitudinal, or single stage), as well as other factors.

For 3315 experiments from 1716 articles, 67% focused on a single stage, 31% were cohort longitudinal and just 1.7% used an individual longitudinal approach.

While life-history stages have been studied extensively, we suggest that the field prioritize individual longitudinal studies to understand the phenotypic correlations among stages.

Richardson EL, Marshall DJ (2023) Mapping the correlations and gaps in studies of complex life histories. Ecology and Evolution PDF DOI

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Can we apply theory developed to understand hermaphroditism in plants, to animals?

Hermaphroditism — a condition where an organism can produce both male and female gametes — is very common in plants and many animals. While the ability to self-fertilise seems like an evolutionary ‘cunning plan’, there are drawbacks. If hermaphrodites only self-fertilise, they run the risk of inbreeding depression, but where survival or mating opportunities are slim, then self-fertilisation is better than not reproducing at all.

Theory does a good job of predicting when hermaphroditism will benefit plants. Interestingly, animals have not received the same attention. George Jarvis and his PhD supervisors Craig White and Dustin Marshall have found that the same theories predicting hermaphroditism in plants can also be applied to animals.

Essentially, strong competition among siblings for resources or among gametes for fertilisation may drive the evolution of hermaphroditism in both plants and animals.

Highly competitive environments can tip the balance towards hermaphroditism, because hermaphrodites can reallocate resources from male to female function (or vice versa) to increase their competitive advantage.

George and his supervisors considered the accepted evolutionary drivers for hermaphroditism in plants and looked for analogues in marine animals.

In plants, species with limited seed dispersal can experience strong competition among siblings for resources, and are more likely to be hermaphrodites. In marine animals, larval dispersal provides an analogous model to test if the same forces are at play.

Larvae released into the plankton travel further than non-planktonic larvae and feeding larvae travel even further than their non-feeding counterparts. Plant theory predicts that hermaphrodites are more common in species where local competition is greatest; in marine animals then, hermaphroditism should be more common in species with non-planktonic larvae.

Similarly, plants pollinated by specialist insects are more likely to be hermaphrodites. In animals, internal fertilisers are akin to plant species with specialist pollinators; competition between gametes is fierce and so an extra guarantee in the form of hermaphroditism should be more common.

George and his supervisors found other analogues between plant and animal theory as well. Smaller plants and plants at higher latitudes are more likely to be hermaphrodites due to increased competition between gametes and rarer mating opportunities respectively. If plant theory holds, the same patterns between hermaphroditism, size and biogeography will be true for animals as well.

The research team set about compiling data for reproductive mode, larval development mode, fertilisation mode, latitude and adult size for 1,153 species of marine annelids, echinoderms and molluscs.

They found theory developed to understand hermaphroditism in plants, predicts many patterns of hermaphroditism in marine animals. Overall, hermaphroditism is generally associated with limited offspring dispersal, internal fertilisation and small body size.

But just to complicate things, George and his supervisors also found that in annelids and molluscs, species that are external fertilizers are more likely to be hermaphrodites when large, but in internal fertilizers the opposite is true.

George, Craig and Dustin feel their results support Darwin’s supposition from over a century ago: hermaphroditism evolves in response to an organism’s life history and ecology —  not the other way around.

This research was published in the journal Evolution.

Theory developed to understand hermaphroditism in plants, predicts many patterns of hermaphroditism in marine animals. In these taxa (top to bottom: annelids, echinoderms and molluscs) hermaphroditism is generally associated with internal fertilisation, small body size and, with the exception of molluscs, limited dispersal. In each graph, the bars represent average (± SE) predicted probabilities of hermaphroditism from standard regressions, and numbers represent the number of species for each mode. Note that scales differ among taxa.
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Macroevolutionary patterns in marine hermaphroditism

Authors: George C Jarvis, Craig R White, and Dustin J Marshall

Published in: Evolution

Abstract

Most plants and many animals are hermaphroditic; whether the same forces are responsible for hermaphroditism in both groups is unclear. The well-established drivers of hermaphroditism in plants (e.g., seed dispersal potential, pollination mode) have analogues in animals (e.g., larval dispersal potential, fertilization mode), allowing us to test the generality of the proposed drivers of hermaphroditism across both groups.

Here, we test these theories for 1,153 species of marine invertebrates, from three phyla. Species with either internal fertilization, restricted offspring dispersal, or small body sizes are more likely to be hermaphroditic than species that are external fertilizers, planktonic developers, or larger.

Plants and animals show different biogeographical patterns, however: animals are less likely to be hermaphroditic at higher latitudes — the opposite to the trend in plants.

Overall, our results suggest that similar forces, namely, competition among offspring or gametes, shape the evolution of hermaphroditism across plants and three invertebrate phyla.

Jarvis GC, White CR, Marshall DJ (2022) Macroevolutionary patterns in marine hermaphroditism. Evolution PDF DOI

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Changing lanes: can we reconcile the ways we measure reproduction so we can make meaningful comparisons across animal species?

Reproduction is perhaps the only truly unambiguous measure of fitness and yet we measure it in different ways. Biologists working on birds tend to measure clutch size as number of eggs per clutch, while mammal biologists focus on litter size measured in mass. These differences only become obvious when researchers want to move out of their accustomed lanes and ask broader questions applicable to a wide range of animal species. One unequivocal measure of reproduction is reproductive mass per year but how often do researchers measure this?

Reproductive mass per year combines the number of offspring per reproductive bout with the mass of the offspring and, importantly, the number of reproductive bouts per year. We know that some species can have a few large offspring and only reproduce once per year whilst other species can produce many small offspring numerous times per year. So which species puts in the most resources to reproduction? Only by combining measures of offspring mass over time can we really compare reproductive effort across species.

How often are all three components of reproductive mass per year – number of offspring per reproductive bout, offspring mass, and the number of reproductive bouts per year – provided for animals?

PhD student, Sam Ginther, is interested in the energetic costs of reproduction and wondered how feasible it would be to collate reproduction data for a wide range of species. Could he translate the existing data into a consistent and biologically relevant measure of reproductive mass per year?

Sam and supervisors Dustin Marshall, Craig White and Hayley Cameron created a ‘systematic map’ of reproductive trait data that exist in online databases. They used this unbiased approach to collate and describe:

  1. how common is the measure reproductive mass per year in databases, and
  2. how well did more ambiguous reproductive measures (i.e., fecundity per bout, fecundity per year, and reproductive mass per bout) represent a truly comparable measure of reproductive effort – reproductive mass per year.

So, can we use other measures as proxies for reproductive mass per year? While most reproductive measures are poor predictors of reproductive effort, reproductive mass per bout is the exception.

Reproductive databases are amazing resources and represent centuries of work in the field of reproductive biology. However, to unlock their full potential Sam and his colleagues feel that the best way forward is to encourage researchers to measure reproduction in a way that allows us to reconstruct reproductive mass per year; that is, tie reproductive measures to temporal- and volumetric-dimensions. But where this is unrealistic in terms of time and effort then measuring reproductive mass per bout is the next best thing.

This research is published in the journal Global Ecology and Biogeography.

dustinmeeg

Avoiding growing pains in reproductive trait databases: the curse of dimensionality

Authors: Samuel C Ginther, Hayley Cameron, Craig R White, and Dustin J Marshall

Published in: Global Ecology and Biogeography

Abstract

Aim: Reproductive output features prominently in many trait databases, but the metrics describing it vary and are often untethered to temporal and volumetric dimensions (e.g., fecundity per bout). The use of such ambiguous reproductive measures to make broad-scale comparisons across taxonomic groups will be meaningful only if they show a 1:1 relationship with a reproductive measure that explicitly includes both a volumetric and a temporal component (i.e., reproductive mass per year). We sought to map the prevalence of ambiguous and explicit reproductive measures across taxa and to explore their relationships with one another to determine the cross-compatibility and utility of reproductive metrics in trait databases.

Location: Global.

Time period: 1990–2021.

Major taxa studied: We searched for reproductive measures across all Metazoa and identified 19,785 vertebrate species (Chordata), and 440 invertebrate species (Arthropoda, Cnidaria or Mollusca).

Methods: We included 37 databases, from which we summarized the commonality of reproductive metrics across taxonomic groups. We also quantified scaling relationships between ambiguous reproductive traits (fecundity per bout, fecundity per year and reproductive mass per bout) and an explicit measure (reproductive mass per year) to assess their cross-compatibility.

Results: Most species were missing at least one temporal or volumetric dimension of reproductive output, such that reproductive mass per year could be reconstructed for only 4,786 vertebrate species. Ambiguous reproductive measures were poor predictors of reproductive mass per year; in no instance did these measures scale at 1:1.

Main conclusions: Ambiguous measures systematically misestimate reproductive mass per year. Until more data are collected, we suggest that researchers should use the clade-specific scaling relationships provided here to convert ambiguous reproductive measures to reproductive mass per year.

Ginther SC, Cameron H, White CR, Marshall DJ (2022) Avoiding growing pains in reproductive trait databases: the curse of dimensionality. Global Ecology and Biogeography PDF DOI

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Carry-over effects and fitness trade-offs in marine life histories: The costs of complexity for adaptation

Authors Dustin J Marshall and Tim Connallon

Published in Evolutionary Applications

Abstract

Most marine organisms have complex life histories, where the individual stages of a life cycle are often morphologically and ecologically distinct. Nevertheless, life-history stages share a single genome and are linked phenotypically (by “carry-over effects”). These commonalities across the life history couple the evolutionary dynamics of different stages and provide an arena for evolutionary constraints. The degree to which genetic and phenotypic links among stages hamper adaptation in any one stage remains unclear and yet adaptation is essential if marine organisms will adapt to future climates.

Here, we use an extension of Fisher’s geometric model to explore how both carry-over effects and genetic links among life-history stages affect the emergence of pleiotropic trade-offs between fitness components of different stages. We subsequently explore the evolutionary trajectories of adaptation of each stage to its optimum using a simple model of stage-specific viability selection with nonoverlapping generations.

We show that fitness trade-offs between stages are likely to be common and that such trade-offs naturally emerge through either divergent selection or mutation. We also find that evolutionary conflicts among stages should escalate during adaptation, but carry-over effects can ameliorate this conflict.

Carry-over effects also tip the evolutionary balance in favor of better survival in earlier life-history stages at the expense of poorer survival in later stages. This effect arises in our discrete-generation framework and is, therefore, unrelated to age-related declines in the efficacy of selection that arise in models with overlapping generations.

Our results imply a vast scope for conflicting selection between life-history stages, with pervasive evolutionary constraints emerging from initially modest selection differences between stages. Organisms with complex life histories should also be more constrained in their capacity to adapt to global change than those with simple life histories.

Marshall DJ, Connallon T (2022) Carry‐over effects and fitness trade‐offs in marine life histories: The costs of complexity for adaptation. Evolutionary Applications PDF DOI

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The Conversation: Why are bigger animals more energy-efficient? A new answer to a centuries-old biological puzzle

By Craig White and Dustin Marshall

This article is republished from The Conversation under a Creative Commons licence.

If you think about “unravelling the mysteries of the universe”, you probably think of physics: astronomers peering through telescopes at distant galaxies, or experimenters smashing particles to smithereens at the Large Hadron Collider.

When biologists try to unravel deep mysteries of life, we too tend to reach for physics. But our new research, published in Science, shows physics may not always have the answers to questions of biology.

For centuries scientists have asked why, kilo for kilo, large animals burn less energy and require less food than small ones. Why does a tiny shrew need to consume as much as three times its body weight in food each day, while an enormous baleen whale can get by on a daily diet of just 5-30% of its body weight in krill?

While previous efforts to explain this relationship have relied on physics and geometry, we believe the real answer is evolutionary. This relationship is what maximises an animal’s ability to produce offspring.

How much do physical constraints shape life?

The earliest explanation for the disproportionate relationship between metabolism and size was proposed nearly 200 years ago.

In 1837, French scientists Pierre Sarrus and Jean-François Rameaux argued energy metabolism should scale with surface area, rather than body mass or volume. This is because metabolism produces heat, and the amount of heat an animal can dissipate depends on its surface area.

In the 185 years since Sarrus and Rameaux’s presentation, numerous alternative explanations for the observed scaling of metabolism have been proposed.

Arguably the most famous of these was published by US researchers Geoff West, Jim Brown and Brian Enquist in 1997. They proposed a model describing the physical transport of essential materials through networks of branching tubes, like the circulatory system.

They argued their model offers “a theoretical, mechanistic basis for understanding the central role of body size in all aspects of biology”.

These two models are philosophically similar. Like numerous other approaches put forward over the past century, they try to explain biological patterns by invoking physical and geometric constraints.

Evolution finds a way

Living organisms cannot defy the laws of physics. Yet evolution has proven to be remarkably good at finding ways to overcome physical and geometric constraints.

In our new research, we decided to see what happened to the relationship between metabolic rate and size if we ignored physical and geometric constraints like these.

So we developed a mathematical model of how animals use energy over their lifetimes. In our model, animals devote energy to growth early in their lives and then in adulthood devote increasing amounts of energy to reproduction.

Animals allocate more energy to reproduction after they reach maturity.

We used the model to determine what characteristics of animals result in the greatest amount of reproduction over their lifetimes – after all, from an evolutionary point of view reproduction is the main game.

We found that the animals that are predicted to be most successful at reproducing are those that exhibit precisely the kind of disproportionate scaling of metabolism with size that we see in real life!

This finding suggests disproportionate metabolic scaling is not an inevitable consequence of physical or geometric constraints. Instead, natural selection produces this scaling because it is advantageous for lifetime reproduction.

The unexplored wilderness

In the famous words of Russian-American evolutionary biologist Theodosius Dobzhansky, “nothing makes sense in biology except in the light of evolution”.

Our finding that disproportionate scaling of metabolism can arise even without physical constraints suggests we have been looking in the wrong place for explanations.

Physical constraints may be the principal drivers of biological patterns less often than has been thought. The possibilities available to evolution are broader than we appreciate.

Why have we historically been so willing to invoke physical constraints to explain biology? Perhaps because we are more comfortable in the safe refuge of seemingly universal physical explanations than in the relatively unexplored biological wilderness of evolutionary explanations.
The Conversation

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Metabolic scaling is the product of life-history optimization

Authors: Craig R White, Lesley A Alton, Candice L Bywater, Emily J Lombardi and Dustin J Marshall

Published in: Science

Abstract

Organisms use energy to grow and reproduce, so the processes of energy metabolism and biological production should be tightly bound. On the basis of this tenet, we developed and tested a new theory that predicts the relationships among three fundamental aspects of life: metabolic rate, growth, and reproduction.

We show that the optimization of these processes yields the observed allometries of metazoan life, particularly metabolic scaling. We conclude that metabolism, growth, and reproduction are inextricably linked; that together they determine fitness; and, in contrast to longstanding dogma, that no single component drives another.

Our model predicts that anthropogenic change will cause animals to evolve decreased scaling exponents of metabolism, increased growth rates, and reduced lifetime reproductive outputs, with worrying consequences for the replenishment of future populations.

White CR, Alton LA, Bywater CL, Lombardi EJ, Marshall DJ (2022) Metabolic scaling is the product of life-history optimization. Science DOI