WE HAVE all seen images of polar bears stranded at sea on chunks of ice. This charismatic species has become a poster child for the devastating effects of climate change. But as the world warms, spare a thought for another group of animals that face a unique challenge. These are the creatures whose entire reproductive future depends on how hot their environment is.
The threat from climate change to animals whose sex is determined by temperature seems obvious. Higher temperatures cause them to produce offspring primarily of one sex, a skew that would appear to put them on the road to extinction. But the curious fact is, this group contains some of the most ancient lineages in the animal kingdom – from crocodiles and turtles to fish and even a reptile-like – and they have survived repeated bouts of global warming in the past.
So how have they made it this far given their apparent sensitivity to temperature? To what extent does the current warming differ from events they have faced before? And should we worry about their survival? Researchers rushing to answer these questions have made some surprising discoveries, including a sexual innovation that might have helped these species survive climate change in the past. This innovation could have been key to the evolution of birds, and even explain why they are the only dinosaur descendants today.
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What’s more, the plight of these species may not be as far removed from us as it seems. There are now intriguing hints that global warming is having an effect on the sex ratios of newborn humans too (see “Girls like it hot”).
For many animals, including the backboneless invertebrates, sex is determined by sex chromosomes inherited from their parents. Among humans and other mammals, for example, most females have two X chromosomes, while males have one X and one Y chromosome. But some fish species and many reptiles, including crocodiles, alligators and marine turtles, take a different approach. They are at the mercy of ambient temperatures, which flick a switch that dictates whether the embryo will develop into a male or a female. In reptiles, the critical period of temperature sensitivity occurs during egg incubation. In fish, it is after hatching, at the larval stage.
There is now abundant evidence that global warming is leading to increasingly unequal sex ratios in these creatures. For most, that means an excess of females. Take most species of marine turtles, which usually hatch as females if incubated at temperatures above 26°C. Many studies confirm that in recent, warmer, years they have produced female-heavy hatchling populations. And projections reveal that the situation could get more extreme very soon. One study, for example, calculated that the proportion of females will rise from the current level of 52 per cent to between 76 and 93 per cent by 2100.
That sounds disastrous, but there are some glimmers of hope. For a start, some of these animals are taking steps to influence their destiny. Female marine turtles, for example, have , when conditions are cooler. What’s more, research published in 2019 reveals that turtle embryos may move around within their eggs to find cooler spots and so . Such strategies can help to reduce the impact of higher temperatures on these creatures.
“Evidence shows warming is leading to increasingly unequal sex ratios”
But there is an even stronger reason to be optimistic that female-biased populations won’t lead to extinction. “An excess of females is actually beneficial,” says Nadav Pezaro at Stellenbosch University in South Africa, “as long as there are enough males to service the entire female population.” There are only so many offspring that each female can produce, so they – not males – represent a limiting factor to population size. As a result, female-biased populations tend to have higher reproductive output than groups with equal numbers of males and females. Some researchers even think that this explains . While other species might struggle to adapt to changing environmental conditions, those that have evolved this mechanism could
The pro-female bias has another benefit too: it is inherently self-correcting. Pezaro and his colleagues have such as crocodilians, a group that evolved perhaps more than 200 million years ago. For these animals, both low and high incubation temperatures produce females, while males are produced at intermediate temperatures. Crucially, individuals differ genetically in the temperature range that triggers male development. So, while the genome of one crocodile might make it male if incubated between 25°C and 29°C, for another the range could be 27°C to 32°C. In a particularly warm year, only embryos carrying genes to produce males in a high temperature range will hatch as male. Once mature, these few males will probably mate with multiple females, making future hatchlings more likely to carry genes that favour male development at warmer temperatures. In this way, mostly female populations can continue to produce a modest reserve of males, helping the population stay afloat and even thrive as temperatures increase.
This tendency to self-correct, together with the ability to produce population booms, could explain how species that produce more females at higher temperatures have survived warming in the distant past. But there is a limit to the adaptability of this mechanism. Eventually, there won’t be enough males to mate with all the females and populations will start declining. Unfortunately, there are as a result of the rapid pace of modern climate change compared with past events. Reptiles are at particular risk because their long generation spans mean they can’t adapt fast enough. , for example, take up to 30 years to reach sexual maturity. And a recent study of freshwater turtles in China predicted that many populations will be within just a few decades.
Global warming poses an even greater threat for another group of species – those in which higher temperatures produce fewer females and more males. Animals with this rarer type of temperature-dependent sex determination include the tuatara, the last member of a reptile-like lineage dating back to the Triassic era, 250 million years ago. Today, most tuatara populations are isolated on a few dozen islands off New Zealand, and Nicki Mitchell at the University of Western Australia thinks we should be concerned for their future. Her research has identified an “We suspect ,” she says. “By 2085, there will be almost no nest microclimates on the island that would produce females, even with radical adjustments to nesting behaviour.”
Tuataras are by no means alone. Fish with temperature-dependent sex determination also produce more males when the going gets hot – the number of species that do it is unknown but it includes commercially important ones such as , . In both freshwater and marine species, the sex ratio can shift from equal numbers to if temperatures rise by just 1°C to 2°C, which is lower than some projections of the rise in global sea temperatures by the end of this century as a result of global warming.
Many of these species have sex chromosomes that would normally dictate whether they become male or female, but temperature routinely overrides these genetic instructions. Some fish, such as Nile tilapia, may be contributing to this effect and fast-tracking the development of a sex imbalance in their own populations. A recent study found that they prefer spending time in warmer waters during their critical period of development, causing many genetically female tilapia to effectively .
A sexual revolution
So how will things pan out for these species as global temperatures continue to rise? Will populations become trapped in a runaway male bias and go extinct? That is certainly a possibility. However, a study by Pezaro and others suggests , one that appears to have been used in the past.
According to their model, a prolonged shortage of females could eventually trigger the evolution of a primitive sex chromosome dictating female development. This might begin with a chance event in which one or more genes become mutated, causing them to switch off the genes that regulate an embryo’s thermal sensitivity. This would prevent it from developing into a male, whatever the temperature. The chromosome carrying these mutated genes would, de facto, become a nascent sex chromosome, obliging embryos that inherit it to become female. Only embryos inheriting two copies of the chromosome lacking the mutated genes would be capable of developing into males.
This is precisely the system universally found in birds, where females have a set of ZW sex chromosomes – where W dictates femaleness – and males have ZZ. According to Pezaro and his colleagues, birds might be a prime example of animals whose ancestors originally had temperature-dependent sex determination, but who evolved a pro-female sex chromosome as a way out of a catastrophic male bias. This, the researchers suggest, could have been triggered by the evolution of hot-bloodedness and egg-brooding behaviour, which maintained incubating eggs at consistent, warm temperatures. The evolution of sex chromosomes might have contributed to the rise of birds in the fossil record some 150 million years ago. Meanwhile, some researchers believe that continued reliance on temperature-dependent sex determination may have Birds are their only descendants alive today.
This evolutionary innovation could also be the saving strategy for today’s species that rely on temperature to determine sex. Some of the fish involved already have sex chromosomes, so the solution for them could be to simply find a way to prevent temperature overriding these. And evidence suggests that turtles have evolved sex chromosomes at least , each one thought to . This gives grounds for optimism that it can happen again.
The major difference this time, however, is that along with rising temperature, the animals face other challenges their ancestors didn’t have to deal with. “Many species have lost the connecting habitat that would have allowed them to shift their distributions to more suitable climates in the past,” says Mitchell. Habitat destruction also reduces population sizes, which can limit the ability to adapt. “The likelihood of harbouring beneficial genetic variants is significantly greater in larger populations,” says Pezaro. “And many of today’s populations are nowhere near the sizes they were at their historic peaks.” That means they have less of the raw material on which evolution can get to work. And even if they can adapt, they may not be able to evolve fast enough if the rate of temperature change outpaces the speed at which they can reproduce.
Here is yet another reason why we need to act now to limit climate change and environmental degradation. Our efforts won’t just help polar bears on thin ice, they will also help turtles, tilapia and tuataras that find themselves in increasingly hot water.
Girls like it hot
As Earth warms, it is affecting the balance of males and females among animals whose sex is determined by temperature. Surprisingly, temperature can also affect human sex ratios. A host of studies show that . What’s more, when researchers in the aftermath of two abnormal seasonal events – the extremely hot summer of 2010 and unusually cold winter weather of early 2011–they discovered that fewer boys were born nine months later in both cases.
At first glance, these findings seem to defy logic. In humans, sex is genetically determined. Embryos that inherit two X sex chromosomes become female and those inheriting an X and a Y become male. Temperature can’t override the genetic instructions we pass down to our children. It can’t switch a genetically male embryo into a female. However, it can influence sex ratios in another way.
Only about 30 to 50 per cent of pregnancies , with most of the rest being miscarried within six weeks of conception. This has been dubbed . And when it comes to survival, . For a start, they fall victim to a host of developmental issues that don’t affect females, because they can’t compensate for any genetic mutation on their X chromosome by relying on a normal second copy. They are also more sensitive to environmental conditions during pregnancy – not just extremes of temperature but a variety of factors that induce stress in mothers-to-be. Women give birth to relatively fewer boys shortly after dealing with catastrophes such as , floods and bouts of , as well as .
Women give birth to fewer boys after dealing with a stressful event
Why male fetuses are more likely to be victims of these events remains a matter of debate. Ralph Catalano at the University of California, Berkeley, thinks for a pregnant woman’s body to reject a child that is less likely to survive under difficult conditions. And he notes that males tend to have weaker immune systems than females, making them at any age. Indeed, many species seem to have evolved a system for aborting male embryos in times of stress and scarcity. Rodents, for example, give birth to fewer males or .
It is estimated that in the aftermath of flood, earthquake or smog. Climate change is increasing the likelihood of some of these stressful events, so in that sense it is having an impact on the sex ratios of human populations. These changes might marginally increase the difficulty of finding a sexual partner in affected regions, but they don’t present an existential threat to humanity as rising temperatures may do to other species.
