fig wasps try to balance sex ratios for survival but they can get it wrong

Television nature programmes and scientific papers tend to celebrate the perfection of evolved traits. But the father of evolution through natural selection, Charles Darwin, warned that evolution would produce quirks and “blunders” that reflect a lineage’s history.

Our recent study from the Kruger National Park in South Africa shows how true this is. Our team of behavioural ecologists found that the behaviour of certain fig wasps, long considered textbook examples of precise adaptation, is far from perfect.

Previous research on fig wasps, but also other parasitoid wasps in general, has focused almost exclusively on design perfection. The aim of our work was to investigate a case where we expected to see “imperfections” due to necessary compromises and the legacy of history.

Our study focused on Ceratosolen arabicus, a tiny wasp (about 2.5mm long) that pollinates sycamore figs. We will call them “pollinators” for simplicity.

For years, researchers have admired how pollinating fig wasps such as C. arabicus adjust the percentage of their offspring that are male (their sex ratios) with near mathematical precision to maximise their reproductive success.

But a previous study suggested that when a pollinator shares a fig with another species of wasp it might incorrectly “adjust” its sex ratio as if it was with a female of its own species.

For our research, we allowed the pollinator to lay eggs on its own or together with a gall wasp (Sycophaga sycomori) or a cuckoo wasp (Ceratosolen galili). These species, like the pollinators, crawl into figs to lay their eggs and may elicit the incorrect response.

We then used a statistical approach to determine how well various hypotheses explained the variation in the data. The hypotheses we tested were:

  • that the pollinators’ sex ratio remained unchanged by the presence of the other species

  • various degrees of effects, for example, that each of the species affects the sex ratio differently.

We found that the other two species of wasps do indeed interfere with the pollinators’ neat sex ratio production mechanism. Pollinators lose up to 5% of their potential grandchildren when they share a fig with a gall wasp, and 12% when they share it with a cuckoo wasp.

Still, the pollinators have survived for millions of years and are not expected to go extinct because of this loss of grandchildren.

Given such a “flaw” in a trait that seemed perfect, biologists should expect to see many “design errors” in life if we look for them. We have to be open to that possibility so that we see what’s actually there and not what we expect to see.

How things work

In each fig, one or a few pollinator mothers lay all their eggs. The mother or mothers’ offspring hatch inside the fig and mate inside. When the mother or mothers’ offspring mature, they mate within the fig, meaning brothers routinely mate with sisters. This means brothers will compete among each other for mating opportunities. In contrast, mated females leave their “birth” fig and disperse to start the cycle anew. But importantly, females compete with unrelated females to find new figs to lay their eggs in.

Therefore, a lone mother should produce just enough sons, about 10% of her total brood, to ensure all her daughters get mated. The rest can be daughters.

The wasps have a simple trick to control the sex ratio directly: unfertilised eggs become sons, while fertilised ones become daughters.

When two mothers lay eggs in the same fig, each must produce more sons, around 25%, because now their sons have to compete with those of the other mother. But if a mother shares a fig with another species, this logic does not apply because competition for mates and mating opportunities for her sons do not change. Therefore, her sex ratio should stay the same as if she were alone.

But it does not.

Pollinator mothers use two simple mechanisms to adjust their sex ratio in response to the presence of other pollinators, but these mechanisms are also triggered by other species.

Let us explain the first mechanism using a gin and tonic analogy.

Imagine a bartender making a G&T: first, he pours a tot of gin (sons) and then fills the rest of the glass with tonic (daughters). Now, imagine two bartenders unknowingly making a G&T in one glass. They both add a tot of gin and then top up with tonic. The result is a stronger drink with more gin.

Pollinator mothers do something similar. They tend to lay male eggs first, and then gradually switch to laying females. We call this the ladies-last effect. But when other species like the cuckoo wasp are present, this pattern still changes the sex ratio because the second species shrinks the glass’s total size. As a consequence the pollinator ends up laying fewer daughters. This can be seen in the figure moving from right to left along the x-axis.

The average clutch composition of a single pollinator mother when she is on her own, with the gall wasp and with the cuckoo wasp. Notice that both the number of daughters decreases and the number of sons increases in the presence of the other two species.
Author supplied

The second mechanism works differently but leads to the same problematic outcome. It relies on an active adjustment of the sex ratio. Although the G&T analogy breaks down, this is like each bartender adding more than a tot of gin when he realises there is a second bartender mixing a drink in the glass.

Similarly, when a pollinator detects another pollinator, she increases the number of sons. But when another species is present, she still behaves as if she is competing with her own kind, increasing her number of sons, as can be seen in the figure moving upwards along the y-axis.

Since both mechanisms continue operating inappropriately when other species are present, the sex ratios become erroneously skewed. Specifically, the sex ratio of a single mother shifts from 10% sons when she is alone, to 16% when she is with a gall wasp, and to 26% when she is with the cuckoo wasp. It should have remained at 10%.

All that glitters is not gold

As an isiZulu proverb says: “Ikiwane elihle ligcwala izibungu”, literally translated to: “The nicest-looking fig is usually full of worms.” Pollinator sex ratio adjustment has been touted as a prime example of how perfectly natural selection can optimise the design of biological systems. But this is an oversimplification.

In reality, the history of a trait and compromises between a trait’s various functions can direct evolution to imperfect solutions. For instance, here evolution did not “design” separate “solutions” for with-own-species and with-other-species scenarios.

Instead, evolution seems to have optimised it for the average condition, an imperfect, but workable, compromise. The cost in number of grandchildren due to this compromise is astronomical because pollinators in the Kruger National Park frequently share a fig with another pollinator, galler or a cuckoo wasp.

Such trade-offs are likely common in nature. Evolution tends not to redesign from scratch; rather, it tinkers with what is already there. As a result, we often get solutions that work well enough, rather than perfectly.

So next time you marvel at a natural wonder, remember: the story is rarely one of flawless design. It is a story of imperfect compromises, shaped by what evolution could do with what it had. And that story is far richer and more real than any Hollywood ending.

by : Jaco Greeff, Professor in Genetics, University of Pretoria

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