Organisms respond to their environment by changing morphology or behaviour, sometimes very dramatically. But our warming climate may be pushing this capacity to its limit.
Among the coral beds in the shallow warm waters of the Great Barrier Reef, a male clownfish dances around the tentacles of the anemone he calls home, his bright orange pectoral fins fanning rhythmically back and forth.
He is rather small with non-functional gonads, and very submissive to the dominant male and female with whom he cohabits. Yet he has the capacity to change this dynamic, and dramatically so: once the female dies, he will take his place at the top of the male social order, growing in size and gaining the ability to reproduce. Meanwhile, the formerly dominant male will undergo a sex change to become his female breeding partner.
Male-to-female sex change is a common twist in the life history of many clownfish. It is an example of sequential hermaphroditism, where an organism changes sex at some point during its lifetime to increase its reproductive prospects. In this case, male clownfish are responding to local environmental stimuli: social and hormonal cues provoke a cascade of developmental, physiological and behavioural changes within the organism.
Sequential hermaphroditism is just one example of organisms modifying their physical or behavioural traits – their phenotype – in response to their environment. Scientists call this phenotypic plasticity.
There are countless examples of phenotypic plasticity in nature, in both plants and animals. It can involve rapid, transient changes within the organism’s immediate repertoire, such as the dramatic colour changes exhibited by octopuses to camouflage themselves from predators.
Plasticity can also include gradual developmental processes leading to more permanent, discrete phenotypes, such as the specialised worker castes of social insects. Whether ants or bees develop into a queen or a forager depends on what nutrients they are fed as developing larvae. This caste specialisation is an example of polyphenism, where two or more distinct phenotypes are produced from the same genotype (set of genes). Polyphenism is common in insects, and is what allows them to morph between different life stages, just as a caterpillar transforms into a butterfly. Which phenotype is produced depends on environmental stimuli, such as seasonal variation in nutrition or temperature.
Context-dependent sex determination is another example of polyphenism, and is important in determining sex ratios in the developing offspring of some species. In sea turtles, temperature is the fate-sealing stimulus, with embryos developing mostly into females in warmer conditions, or mostly into males when exposed to cooler temperatures.
Learning is yet another plastic trait important to many animals’ long-term survival. Individuals adjust their behaviour in response to their environment ‒ by avoiding certain noxious foods, evading predators, or learning to forage or build viable nesting sites.
We now understand that almost all traits are plastic to some degree. This makes sense given that an organism’s environment is inherently variable, so to ensure optimal survival and reproductive outcomes their traits should act as a fluid and malleable buffer against changing conditions. But there may be trade-offs and limits to plasticity, and organisms will vary in how plastic they are.
"Presumably the maintenance of the machinery that allows an organism to change its phenotype comes at some cost," says Assoc Prof Adrienne Nicotra, a reproductive ecologist and evolutionary ecophysiologist at Australian National University.
"So it only makes sense to have the potential for plasticity […] within an environment that is variable on a particular scale, otherwise you’re better off producing the perfect phenotype and sticking with it.”
At one end of the spectrum are specialists, who can only survive within a narrow range of environmental conditions. At the other end are generalists, who thrive under a variety of scenarios. The success of either strategy is context dependent. In a rapidly changing environment, specialists are vulnerable with limited ability to adapt. However, if conditions are stable and predictable, specialists tend to outcompete their generalist counterparts. In this context, plasticity comes at a cost to generalists: they are "jacks-of-all-trades but masters of none".
Phenotypic plasticity is especially important for immobile organisms like plants, which can't simply move away from unfavourable environments. Instead, they must change their form to cope as best they can.
“Something about plants that we often forget is that they’re modular," says Nicotra. "So each leaf is an individual organ, and a plant can make one kind of leaf in spring and a different kind of leaf in summer and autumn, and then the old ones die and fall off. It’s not like we can remake our hands if they fall off.”
Phenotypic plasticity is now a booming area of research. In the last five years alone, there were almost 1000 research papers that included the term in their title, compared with just two papers in the period 1970‒1974.
“It’s remarkable – it is increasing absolutely exponentially,” says Nicotra. “It’s moved from being a subject of interest of a few evolutionary biologists to something that is very widely discussed.”
This rising interest in phenotypic variation is a game-changer of sorts, underpinning a scientific revolution that is moving away from the gene-centric evolutionary dogma that once held sway, towards a more dynamic understanding of the complexity and diversity of life.
Legendary Harvard biologist Stephen J. Gould anticipated this new wave of understanding, writing in the New York Times: “The collapse of the doctrine of one gene for one protein, and one direction of causal flow from basic codes to elaborate totality, marks the failure of [genetic] reductionism for the complex system that we call biology.”
Linear notions of genetic reductionism have been hard to shake. But we have known for a while that a single genome has the potential to give rise to a variety of phenotypes in response to the environment. We only have to look to identical twins to know that this is the case: while sharing the same genes, twins may differ markedly in personality, health and appearance.
The concept of the temporally plastic organism, mediated by the environment, has inspired researchers to expand beyond the nature-nurture dichotomy, to pool and integrate across many once-siloed areas of knowledge, including genetics, ecology, developmental biology and evolutionary theory.
A fresh understanding of phenotypic plasticity is becoming ever more important, as it may help us understand how individuals, populations and species can respond to a changing environment.
Arguably the biggest environmental challenge we face today is rapid climate change. With researchers having accepted its inevitability, the focus now is on how organisms can adapt – and quickly. Where the process of genetic adaptation is too slow to keep up, phenotypic plasticity might be critical to how organisms cope.
“Climate change is bringing a combination of resources and conditions that organisms haven’t seen before," says Nicotra, "and when you impose that novelty, you can get a novel phenotype being expressed, and then that can be under selection. So it can expose material for rapid evolution in unpredictable ways."
Scientists are particularly interested in whether phenotypic plasticity in combination with genetic variation is adaptive (fitness-enhancing) or maladaptive (fitness-reducing) under variable environmental conditions.
Rising temperatures are already threatening sea turtle populations globally. In this case, temperature-dependent sex determination is maladaptive, with higher temperatures skewing sex ratios to such a degree that populations have very few breeding males, ultimately leading to population decline.
Managing and restoring plant or animal populations vulnerable to changing environments usually involves increasing their ability to tolerate change. This is often done by introducing individuals with a high amount of plasticity who are more tolerant of variability and allowing them to intermingle with those who have less plasticity, making for a more robust population overall.
Researchers are now using a combination of lab and field-based approaches to study phenotypic plasticity, and to understand what phenotypes might be more resilient to changing conditions.
Nicotra and her colleagues are researching native plants in the Australian Alps, which provide a useful simulation of climate change. Study sites at low altitude indicate what higher altitude sites and their organisms might look like in a generation's time.
“The plants that are found in those lower elevation sites encounter more variable environments compared to plants of the same species at higher elevations," says Nicotra. "We’re finding that those plants are more plastic, and that plasticity helps them maintain their performance and produce good numbers of seeds."
So phenotypic plasticity may allow some species to cope with the effects of a warming climate, at least in the short-term. Nicotra is optimistic, but cautious about treating it as an easy fix to our problems.
“It’s important when we’re talking about the potential of species to buffer against climate change to remember that it’s limited – plasticity isn’t perfect,” she says. “I think some species will adapt, and some won’t – the challenge facing us now is to figure out how we predict the winners and the losers, and do what we can to conserve the losers in some way."