Why Insects Cannot Stand the Heat of Climate Change

Climate change is gripping our planet. News headlines proclaim warmer winters and hotter summers, and these changes are impacting Earth’s biodiversity. Have you ever wondered how climate change causes extinctions? This is an important, ongoing research question because understanding how heat impacts living organisms could help us predict how species will cope in a warmer world and give us the knowledge we need to help vulnerable organisms. Insects make honey, pollinate crops, control pests, and recycle waste into nutrients. Despite being numerous and often helpful to humans, insects, and the effects that climate change is having on them, are often overlooked. Due to climate change, heatwaves are becoming more common and intense. In this article, we explore the impact of simulated heatwaves on a beetle species in the laboratory. Keep reading to learn about how heatwaves could cause damage that lasts over generations, potentially leading to extinctions.

extreme weather event. A heatwave can be defined as days in a row with temperatures • C hotter than historical averages. In the future, heatwaves will be even more common and intense. To cope with heatwaves, people and animals must change how they live. If they fail to do so, species may face severe consequences, including stress or even extinction.
For decades, as Earth has warmed, we have seen nature respond to the stress of higher temperatures. Some species have shifted where they live and when they reproduce, while others have changed how they live (Figure )  Scientists are still researching the responses of species to climate change, so this table will likely keep changing over time as we learn more. further up mountains or toward the poles, searching for cooler areas. Many insects have become smaller and lighter in color to cope with higher temperatures. However, if warming is too great or happens too quickly, species risk extinction. Some organisms, like coral, are very vulnerable because they are slow to grow and move. Others, like polar bears, have shrinking habitats and nowhere else to go. It has already been too late to save some species, like the golden toad, from extinction due to climate change.

HOW DOES CLIMATE CHANGE CAUSE EXTINCTIONS?
Humans are face drastic changes to Earth's weather due to climate change, including droughts, flooding, and unusual rainfall; and extinctions due to climate change are already happening. In , scientists realized that very few studies on climate change (only in ) investigated how climate change causes extinctions [ ]. Learning how climate change impacts Earth's species will help us predict how those species will cope in the future. This knowledge will also help us focus our e orts to help vulnerable life forms as their habitats change.
The idea for our study came from some research reporting that short and unnatural heat shocks damaged reproduction in male humans and farm animals. We thought that, with rising temperatures, male reproduction could be negatively a ected. To test this hypothesis, we exposed an insect species to simulated heatwaves in a laboratory. We studied whether damage to reproduction occurred after heat exposure, and whether it could be repaired after a certain time.

WHY STUDY INSECTS?
Despite existing in huge numbers and making up about half of all species, insects are often overlooked. Many insects are helpful to us; they pollinate crops, produce fertilizer, and make foods like honey. They are also very important for the planet's health because they are food for larger animals and they help to control certain pests. Insects are "cold blooded," so they need external warmth to be active. However, too much heat can be damaging. This makes certain insects good model animals to use in laboratory experiments exploring the impact of heatwaves. Hopefully, laboratory findings like ours can help inform conservation e orts for vulnerable life forms and biodiverse ecosystems.

PUTTING THE HEAT ON MALES
Several years ago, red flour beetles (Tribolium castaneum) were caught in the wild. These beetles can be grown in dishes filled with flour, yeast, and oats. At • C, it takes a month for an egg to develop into a To explore the impact of heatwaves, males and females were separated during the cocoon stage, to make sure they could not mate. This research looked at males, which were kept at either the normal • C or given a -day, • C "heatwave". We chose • C because this is the summer heatwave temperature in over countries. Afterwards, the survival of heated and unheated males was compared. Each survivor was paired with an unheated female, for a chance to mate. The success of mating behavior was recorded, and the male beetles were dissected so their reproductive organs and sperm could be examined with a microscope. After mating, the females were isolated in flour until they produced o spring, which were then counted. We looked at the impact of heatwaves on o spring health and lifespan, and male o spring fertility. The number and quality of o spring produced is important for success in nature.

MALE REPRODUCTION CANNOT STAND THE HEAT
We found that heatwaves damaged various aspects of male reproduction ( Figure ). First, we saw that males exposed to heatwaves had worse mating behavior, being less likely to start and slower to finish it. Heat exposure also shrank the size of males' testes, which limited sperm creation. Heated males created % less sperm than unheated males, and half of the sperm produced were dead! After heated males transferred sperm packets to females, only half the number of sperm were stored inside her, compared to packets from unheated males.
Females mated to heated males laid fewer eggs, and the eggs they did produce were half as likely to hatch. It may be that sperm from heated males were unable to fertilize eggs, or that the heat damaged genes and caused the embryos to stop growing, or both. Concerningly, heatwaves experienced by adult beetles caused long-term damage to the health of unheated o spring [ ]! On average, unheated flour beetles live for around a year, but o spring from heated fathers died weeks earlier! Male o spring from heated fathers were slower at mating, less likely to fertilize females, and created fewer o spring from successful matings.

INSECT LIFE STAGES MATTER!
The findings described above were all from heating adult beetles. However, insects have a complex life cycle in which big changes happen in stages; think about caterpillars becoming butterflies, for example. We wondered whether these very di erent life stages might

LIFE STAGE
A life stage is one part of a complex life cycle. For example, beetle growth changes drastically from ova (eggs) to larvae (grubs), then pupae (cocoons), followed by imago (adults).
respond di erently to heat stress. We compared the response of  Figure   Heatwaves can impact a series of traits in male insects, which vary depending on the life stage exposed. Heatwaves were most deadly for beetles at the egg or cocoon stage. Heated adult males had damage to their testes, sperm quantity, and sperm quality. This reduced males' ability to fertilize eggs, and the number and health of o spring produced. Impacts were even seen in grand-o spring production! The seriousness of damage is shown by the amount icons are reduced in number or size. Grey bars display traits for life stages which were not practical (light), or possible (dark), to measure.
We found that heatwaves killed all eggs and cocoons, showing these are the most vulnerable life stages. The heat might have impacted the sensitive developmental changes occurring during these stages. Most mature adults survived heatwaves, probably thanks to their thick shells. Surviving male grubs, young adults, and mature adults were then given females to mate with. As expected, heated mature adults created half as many o spring. Interestingly, heating sterilized young adults (making them completely unable to produce o spring), while it did not hurt the reproduction of grubs! This pattern may be linked to sperm production. Young sperm could be heat resistant, middle-aged sperm could be very vulnerable, and old sperm could be somewhere between the two.

COULD INSECT REPRODUCTION COPE IN A WARMER WORLD?
Our results show that heatwaves cause alarming damage to insects, particularly to the reproductive functions of males at immature life kids.frontiersin.org February | Volume | Article | stages. We wondered whether beetles could adapt by increasing their defense against heatwaves. So, we tested whether heated males were more resistant to a second heatwave. The process by which stress causes changes in an individual that make it more resistant to future stress is called hardening. Unfortunately, the second heatwave HARDENING Process by which stress causes changes in an individual that protect that individual from future stress.
was even more damaging for males, showing that hardening did not happen.
On the bright side, however, we found that heatwave damage was not permanent. Males showed resilience, meaning they could recover

RESILIENCE
The ability of an individual to repair damage caused by stress, if given su cient recovery time.
to the way they were before heating, possibly through the processes cells use to repair themselves after an injury. We tested this by mating heated males with females every days after a heatwave. Some of the males' reproductive functions recovered to normal levelsdays after the heatwave (Figure ). Repair was even possible for males that had been sterilized by heat, such as those that were heated twice or heated while they were young. Other experiments showed that females could cope with the risk of mating with a heat-damaged male Figure   Figure The reproductive functions of male beetles can recover after heatwave damage. Recovery takes, at most, days of rest. (A) A heatwave can shrink testes by almost half, but they can return to normal. (B) Heatwaves can temporarily reduce sperm counts and sperm survival to less than half of expected. (C) Previously heated males do not show protective hardening when they are exposed to a second heatwave; their o spring production is still damaged. However, neither male age or hardening status a ect the recovery of males' o spring production. Small dots show datapoints, and large dots are averages.

WHAT DO OUR FINDINGS MEAN FOR THE FUTURE?
Our experiments demonstrate that the high temperatures currently seen in nature can kill young insects, reduce male reproduction, and cause damage that lasts across generations. We found that damage increases with higher temperatures and longer heatwaves. Since we used a beetle species in our studies, it is likely that our results are similar to what would happen in the wild. Recently, studies have found that males of other insects, like moths, bees, and flies, are also vulnerable to heat. Moreover, research combining data from multiple studies found that temperatures at which male insects are fertile (rather than temperatures at which they can survive) are better predictors of where those species live [ ]!
As global warming and heatwaves worsen, natural populations will shrink over time because fewer individuals survive and reproduce. This could explain some local extinctions that have already been witnessed. Importantly, the vulnerability of insect species has knock-on e ects up the food chain, because the birds and animals that normally eat insects could starve in the absence of insect populations. Although this loss of insects and biodiversity is concerning, there is still hope since it seems possible for life forms to recover from and adapt to heat. Humans can help by conserving their present habitats, giving them access to cooler areas, and doing our best to limit climate change.

ACKNOWLEDGMENTS
The study was supported in the UK by a Natural Environment Research Council (NERC) project grant (NE/K / ) and NERC EnvEast DTP studentship (Award Ref: ). We dedicate this paper to Prof. Matthew J. G. Gage, who started and supervised this research, which now continues in his memory.
. Fertility and mortality impacts of thermal stress from experimental heatwaves on di erent life stages and their recovery in a model insect. R. Soc. Open Sci. : . doi: . /rsos.

CONFLICT OF INTEREST:
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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MELODY, AGE:
Melody is a young activist and climate justice warrior with hopes to change the world day. She has lived in Europe and Australia, and enjoys reading and writing. Melody also enjoys playing and talking to her siblings and friends.