Female beetles become more fertile when very masculine males aren’t around

Cecilia Grimaldi
21st July 2021

The invisible arm race between natural and sexual selection has been shaping the evolution of animal species in ways that scientists could never prove so far. Now a new research shows that, by feeding on the more masculine males, predators can revert the evolution of male sexual traits and indirectly increase female fertility in flour beetles.

Horned flour beetles are uninvited guests of countless kitchens worldwide, where they feed on cereal stocks. Going against the tide, the evolutionary biologist David Hosken warmly welcomes the pest in his lab at the University of Exeter. A choice that has proved far-sighted. 

Using the species Gnatocerus cornutus, Hosken and his colleagues from Okayama University showed that male beetles that encounter a predator evolve less masculinised bodies, thus reducing their chances to mate. Quite surprisingly, the same process also causes the evolution of more fertile females.

These findings are the first experimental evidence of how natural selection (here mimicked by predation) and sexual selection (acting on masculine traits) interact to define species’ evolution – something scientists could only hypothesise so far.

“When most people think about evolution, they think of Charles Darwin’s theory of natural selection,” says Robert Knell, an evolutionary ecologist at the Queen Mary University of London, not involved in the research. But the whole scenario is way more complex.

Different forms of selection shape evolution, and they rarely act on a single trait at a time. For their part, traits nearly always relate to each other, sometimes even in conflictual ways. Thus, theories aren’t sufficient to fully explain how species evolve in response to selection. Field experiments are essential yet challenging to perform when the variables are so numerous.

Horned flour beetles have now helped to tackle this vicious circle. “This is one of the most striking studies I have seen on this matter,” Knell says about the research published June 8 in the journal Nature Communications.

NATURAL, OR SEXUAL SELECTION, THAT IS THE QUESTION

When Darwin wrote the theory of natural selection – which holds that individuals better suited to the environment have higher chances to survive and pass their genes on – he soon realised that something didn’t quite add up.

Large ornaments like the long and colourful peacock’s tail or the massive horns displayed by some antelopes are energy demanding and quite impractical to escape predation. Not to mention the double-edged sword of mating calls that attract predators and parasites. Yet, these characteristics accumulate in populations despite natural selection.

The reason lies in the advantage that these features provide in mating competition – a concept Darwin named ‘sexual selection.’ “Selection is all about how many offspring one produces,” Knell says. “It doesn’t matter how long you live if you are unable to pass your genes on.”

Male horned flour beetles are a textbook example of sexual selection in action. While both genders possess reddish-brown and shiny bodies, only males show off a pair of enlarged and horn-like mandibles. These structures work as weapons during male-male fights for mating, and the larger the mandibles, the higher the chances to win (and thus mate). The flip side is that too large mandibles transform a ladies’ beetle into a slower and easy-to-catch prey, something that natural selection does not tolerate. How exactly do these conflicting pressures play out in evolution?   

Current theories predict that sexual selection exaggerates traits beyond their naturally selected ideals until natural selection kicks in and halts extreme variations. “But there has been no experiment to test the evolutionary outcomes of these theories,” Hosken says. At least until now.

To study the effect of natural selection on mandibles, the researchers used the assassin bug Amphibolus venator. Predation is a major mechanism of natural selection in the wild, and this bug feeds on various pests, including flour beetles.

The scientists sneaked five bugs into a population of hundred male beetles and let the hunting last for two weeks. They then transferred the survivors into a group of females and analysed their progeny throughout eight generations. They observed that their male offspring evolved smaller mandibles than those of control beetles that never met the bug. The reason? Natural selection by predation had preferentially removed the larger-horned and slower males from the first population, thus reverting sexual selection. “These findings are consistent with evolutionary theories,” Hosken says.

What surprised the biologist, though, was “how strongly natural selection on males ultimately affected female fertility.”

A SEXUAL COLD WAR

By analysing female offspring across the same eight generations, the team saw that they gave birth to 20% more offspring than those that mated with males never selected by predation.

Natural selection on males thus affected the fitness of both sexes but in opposite ways: it reduced males’ ability to fight for mating while increasing females’ fertility. “We have not seen that kind of experimental results before,” Knell says.

This clash between the evolutionary interests of the two sexes is known as ‘sexual conflict.’ The phenomenon, first theorised in the 1970s, adds further nuances to Darwin’s evolutionary models and depends on genetically inherited material. 

In male beetles, larger mandibles associate with what scientists call a ‘masculinised body,’ which includes a larger head (to support the mandibles) and a smaller abdomen. “If you select for masculinised males, as sexual selection does, you obtain more masculinised daughters because they share the genes for masculinisation with their father,” says Hosken. Even though masculine females never develop mandibles, they still evolve a smaller abdomen that can host fewer offspring. Predation on masculine males thus leads to the evolution of fittest females.

Although the study lucks some real-world variables to see how the beetles would adapt to these conditions, it is still “adding to our understanding of how sexual selection can impact population-level processes like adaptation to new environments and extinction,” Knell says.

SEXUAL SELECTION AND ADAPTATION

Only in the last few decades scientists realised that sexual selection might be even stronger than natural selection. “Large sexual traits reflect the genetic quality of the animal, and the species where males advertise themselves seem to evolve faster than those where mating is more random,” Knell explains.

And there is more to sexual selection than just male ornaments. “Increasing evidence shows that strong sexual selection also occurs in females and in species with no sexual dimorphism,” says Andrew Knapp, a researcher at the Natural History Museum in London.

Ultimately, whether sexual selection is adaptive remains controversial. “There is increasing evidence that sexual selection can improve the population’s persistence,” Knell says, “but when you are adding phenomena like sexual conflict, it changes the way things happen.” This study, for instance, shows that due to sexual conflict, the population’s extinction risk might increase if the beetle’s predators disappeared, Hoshken adds. 

But to understand extinction, one should study extinct species. “Looking at just living things tells you nothing about extinction. All we see are things that survived,” Knapp argues. Together with Knell, Knapp is now studying sexual selection in dinosaur fossils.

Identifying sexually selected traits without being able to look at animal behaviour is a very challenging task, and “we are quite in the early days,” says Knapp. But their first findings looking at the species Protoceratops andrewsi (a predecessor of the more familiar Triceratops) seem encouraging.

“If you could identify sexually selected traits in extinct species, you could then ask whether species with strong sexual selections persisted longer in the fossil record,” Knell suggests. “And you could apply that knowledge to the massive extinction happening on the planet right now and try to predict which species are more likely to be severely affected by things like climate change and habitat loss.”

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Cecilia Grimaldi owns a doctoral degree in cell and developmental biology and she is now a science communicator in the making here at Imperial College. To sate her hunger for science and writing, she works as freelance writer and blogger for different science-related platforms. Reaching out to the general public is her main interest, as she believes there is a potential scientist inside each curious Homo sapiens after all.