Mainstream evolution theory suggests that genes and the environment shape how organisms look and behave, but how they grow up also matters.
Dr Isabel Smallegange, Senior Lecturer in Population Biology, explores how development shapes fast or slow lifestyles in animals and how this could change our understanding of evolution.
Contents
- What is the gene-centred view of evolution?
- What does the new development-centric evolutionary theory mean?
- Why do animals differ in their ‘pace-of-life syndrome’ (POLS)?
- How POLS shapes species' response to environmental change
- The role of development in evolution
- Defining evolution
- The role of plasticity in evolution
- Conclusion
What is the gene-centred view of evolution?
The gene-centric view of evolution assumes that genes in interaction with the environment determine how living organisms look and behave. This theory is also known as gene selection theory, gene’s eye view, or the selfish gene theory. However, this theory doesn’t consider how an organism’s developmental processes and activities can influence evolution. Sometimes the way an organism develops or interacts with its environment can change its traits – or phenotypes – in ways that don’t match its genotypes.
What does the new development-centric evolutionary theory mean?
A new development-centric theory of evolution emphasises the crucial role that an organism's developmental processes play in shaping its traits and influencing the direction of evolution. This new theory suggests that development is not just a passive process but actively guides how evolution occurs.
This theory of evolution is controversial because it takes genes as only one of many resources that construct phenotypes. However, as an alternative conceptual framework, it can help increase our understanding of unexplained biological phenomena.
Why do animals differ in their ‘pace-of-life syndrome’ (POLS)?
One intriguing biological phenomenon is that animals differ in their pace-of-life syndrome. Pace-of-life syndrome (POLS) refers to a set of linked phenotypic traits related to life history, behaviour, and physiology.
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Figure 1. Examples of species that have a fast pace-of-life, like rabbits, which produce many offspring but suffer high mortality, and a slow pace-of-life, like elephants, which produce only a few offspring in their lifetime but suffer low mortality.
Current gene-centric evolutionary theory is unable to explain why POLSs exist. In a recent paper published in Evolution Letters [1], Anja Guenther and I present a development-centric theory to explain the existence of POLSs.
Our theory links an organism’s pace of life to how it allocates energy based on its level of energy acquisition. It helps explain why current, gene-centric POLS theory fails to predict which animals along the POLS spectrum are most resilient to environmental change.
How POLS shapes species’ response to environmental change
The gene-centric perspective predicts that less fecund, long-lived, and competitive slower-paced animals are more responsive to environmental change because they can invest into moving to new areas and changes in their behaviour [1].
In contrast, the development-centric perspective predicts that faster-paced animals are more responsive because they have a higher energy budget. This allows them to invest more into moving to new areas and changing their behaviour [1].
However, when environmental change is drastic, such as in a sudden but persistent drop in food availability, only slow-paced animals will survive because they have low maintenance costs, unlike faster-paced animals.
Field studies show that slower species are often more threatened than faster ones. If this means that they are also more sensitive to environmental change, it supports the development-centric view.
Ultimately, empirical testing will determine whether faster or slower populations are most sensitive to environmental change. This will be the ultimate test of which mechanism (trade-off between current and future reproduction of gene-centric theory, or selection on the full life cycle of development-centric theory) drives POLS evolution.
The role of development in evolution
The idea that development, not genes, is the main driver of the evolution of traits and trait syndromes has implications for many scientific fields, reshaping how we study and understand evolution.
This idea is controversial and not widely accepted by the scientific community. But it can be productive and insightful to explore new and alternative ways of explaining and defining evolution.
Defining evolution
Undergraduate textbooks define evolution from a gene-centric perspective.
For example, Stearns & Hoekstra [2] state that evolution by natural selection occurs in traits because of three sub-processes:
- Traits vary among individuals
- Trait variation affects how well those individuals survive and reproduce
- Some of this trait variation is determined by genes that also vary among individuals
The survival and reproduction of successful individuals cause the frequency of the genes and the traits that they determine to increase in the next generation. As this process continues over generations, the population becomes better adapted and the inheritance of the adaptive change is reflected in changes in the genetic composition of the population [2].
Lala et al. [3], in Evolution Evolving, state that the above definition assumes the three subprocesses are ‘effectively autonomous’, meaning that they influence each other without changing how they work [3]. However, developmental mechanisms do more than just generate variation (subprocess 2 above); they also modify the processes involved in survival, reproduction, and heredity. As a result, these subprocesses underlying evolution by natural selection become interconnected [3].
Lala and supporters of the Extended Evolutionary Synthesis (ESS; see e.g. [4]), propose a new way of thinking about evolution – one that starts not by seeking the simplest explanation, or the universal one, but a new account of the central role that developmental processes play in evolution.
The role of plasticity in evolution
In Developmental Plasticity and Evolution [5], Mary-Jane West-Eberhard argues that the developmental mechanisms allowing organisms to adapt to their environment are key drivers of adaptation and diversification. But two decades after its publication, the significance of development in explaining adaptive evolution is still not fully recognised [6].
I argue that this is partly because plasticity is viewed from both a gene-centric and development-centric perspectives [8].
From a gene-centric perspective, developmental plasticity functions to anticipate future conditions and the expression of phenotypic traits of animals are taken to be determined by genotype-specified reaction norms.
From a development-centric perspective, developmental plasticity mitigates current stress conditions, generating new and long-lasting phenotypic trait variation.
These different types of developmental plasticity are caused by different factors and will lead to different changes in traits as the environment changes [7,8]. These different evolutionary trajectories will in turn fuel different population dynamics [8].
To be able to predict how organisms respond to environmental change through plasticity, we must explore how developmental processes can facilitate or constrain evolution. For example, most interventions to reduce species extinction risk under global warming are short-term as they aim to buffer organisms from heat stress. But global warming is long-term. Development-centric approaches can redefine how we apply interventions to warming, favouring long-term solutions of evolution and adaptation to warming over short-term ones that buffer organisms against heat stress.
Conclusion
In recent decades, we have discovered numerous extraordinary aspects of the natural world that deserve inclusion in biology’s fundamental theory of evolution.
A development-centric perspective could transform the field of evolutionary science. It could encourage interdisciplinary collaboration by scholars from fields including bioscience, evolution, psychology, mathematical modelling, and philosophy of science. This new way of seeing evolution opens the door to new research opportunities and possibilities to solve real-world problems. It contributes to a more refined and nuanced understanding of evolutionary processes.
You might also like
- read the paper: Smallegange IM, Guenther A. 2024. A development-centric perspective on pace-of-life syndromes. Evolution Letters, qrae069
- find out more about Dr Isabel Smallegange, Senior Lecturer in Population Biology at Newcastle University
- explore biology research from our School of Natural and Environmental Sciences
- read the latest biodiversity blog posts from our researchers
Glossary
Acquisition
Collection and consumption of resources from the environment.
Development
The process by which organisms grow and develop, from a young juvenile to a reproductive adult.
Developmental plasticity
A common natural occurrence where individuals change their development based on internal or external signals. This helps them prepare for future environmental conditions or reduce current stress, leading to lasting changes in their phenotype.
Development-centric perspective
Assumes that natural selection favours developmental systems that tend to construct phenotypes that are successful, relative to other variant systems, at surviving and reproducing.
Fast-paced types
Individuals that grow fast and large, have high reproductive rates, and have high total fitness. At high population densities, their maintenance costs will exceed their total amount of assimilated energy and they will be outcompeted by slow-paced types.
Gene-centric perspective
Assumes that phenotypes evolve because some traits, determined by genes, give individuals a better chance to survive and reproduce.
Pace-of-life-syndrome
Comprising suites of correlated life history, physiological and behavioural traits emerging from different solutions to life-history trade-offs.
Phenotypes
A phenotype is the set of observable characteristics or traits of an organism, such as its appearance, behaviour, and physical features.
Slow-paced types
Avoid impairment at high densities because they have lower maintenance costs, but their growth and reproduction are intrinsically slower than that of fast-paced types, lowering their total fitness.
References
1] Smallegange IM, Guenther A. 2024. A development-centric perspective on pace-of-life syndromes. Evolution Letters, qrae069, https://doi.org/10.1093/evlett/qrae069
[2] Stearns SC, Hoekstra RF. 2005. Evolution: an introduction. Oxford University Press, Oxford.
[3] Lala KN, Uller T, Feiner N, Feldman M, Gilbert SF. 2024. Evolution Evolving: The Developmental Origins of Adaptation and Biodiversity. Princeton University Press, Princeton.
[4] Laland KN, Uller T, Feldman MW, Sterelny K, Müller GB, Moczek A, Jablonka E, Odling-Smee J. 2015. The extended evolutionary synthesis: its structure, assumptions and predictions. Proceedings of the Royal Society London: Biological Sciences 282: 20151019.
[5] West-Eberhard MJ. 2003. Developmental Plasticity and Evolution. Oxford University Press, New York.
[6] Uller T, Milocco L, Isanta-Navarro J, Cornwallis CK, Feinder N. 2024. Twenty years on from Developmental Plasticity and Evolution: middle-range theories and how to test them. Journal of Experimental Biology 227, jeb246375.
[7] Deere JA, Smallegange IM. 2023. Individual differences in developmental trajectory leave a male polyphenic signature in bulb mite populations. Peer Community Journal 3: e117.
[8] Smallegange IM. 2022. Integrating developmental plasticity into eco-evolutionary population dynamics. Trends in Ecology & Evolution 37: 129-137.
