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Mama’s boys: How fig wasp mothers protect their sons

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Fig wasps inside a fig. The love-children of an insect-plant romance.

I recently read this paper about fig wasps. Then I took some aspirin, put a cold press to my head, and had a nap. You may have seen my one other post about plants, so you might already know about my deep-seated distrust of the vegetable kingdom, rooted in my lack of understanding of plant biology.

The paper by Hui Yu and Stephen G. Compton was published in PLoS One. But it’s more than just a scientific paper. It’s a love story: fig and wasp, destined to be together and mutually dependent on each other for continued survival. It’s also about the love of a mother for her sons. And every love story has its tragedy. In this case, it’s the free-loading enemy wasps that kill the love-children of the wasp/fig romance and force the wasp mother to choose which children to protect.

I had a pretty good grasp on the animal side of this interspecies sex story: female fig wasps (who have to lay their eggs inside of figs–I’ll get to that in a bit) lay eggs containing sons in flowers that end up closer to the center of the fig. This leaves the daughters on the periphery where they are more exposed to attacks by enemies. Protecting the boys ensures that there will be enough males in the next generation, since males are naturally rarer than females.

But what’s all this fig business?

[figs]

The nice thing about plants: you can post pics of their genitals without it being called porn! Photo by RHiNO NEAL via Flickr.

Figs and wasps: Intertwined interspecies reproduction

This is where my headache came in. Figs have a complicated reproductive strategy, entirely dependent on tiny little wasps to do their sexy-time business for them.

The fig is a kind of inverted flower bed, with thousands of tiny flowers lining the inside. ‘Female’ flowers can each either produce one seed or nurture one growing wasp larva. A female wasp enters the fig through a small opening, losing her wings and antennae in the process. Don’t worry, she doesn’t need them anymore. She walks around on the flowers, dropping pollen from her birth-fig into the female flowers. Artificial insemination may be relatively new for humans, but figs have been relying on it for a very long time (evolution, you think of everything!). Pollinated flowers will develop seeds, and the circle of life continues.

Laying an egg inside an ovule in the flower’s ovary causes an overgrowth of the ovule tissue (called galling), which will nourish the developing larva. Mama wasps usually deposit eggs only in flowers with short styles–the tube leading to the ovary–because they can’t reach down into long styles with their short ovipositors (egg-depositors). Having variation in the length of styles within a fig fruit guarantees that some flowers will produce wasps and some will produce seeds; this scheme falls apart if you only get one or the other.

Parts of a flower. This shows the boy and girl parts on the same flower, but figs usually have separate male and female flowers. Wasps lay their eggs in the ovary and cause a gall to form in an ovule, which nourishes the developing larva. The style is the tube-like structure connecting the ovary to the stigma. Female wasps can't reach down into the ovary if the style is too long, so they lay their eggs in flowers with short styles. Image Via Wikipedia.

Once the larvae develop, the males emerge first. They escape the galled ovule by chewing a hole to get through it. Then, they chew a hole in the galls containing female wasps and deposit semen, starting the next generation (check out this PBS video link if you want to see males in action). Later, the males will return to facilitate the escape of the females, opening up their galls for them. This helps explain the relatively low number of males: you only need one, theoretically, to mate with all the females and make an exit hole in the fig.

Ants on the outside of a fig, waiting for the unsuspecting fig wasps to emerge. Yes, that little black dot that the ants are fighting over is a fig wasp--look how tiny!

The females then walk around on the male flowers a little bit, picking up lots of pollen to bring on their journey. The male wasps’ final task is to chew an opening in the fig for the females to escape. The ladies then have about 48 hours to find a fig with female flowers and pollinate it. The boys die soon after leaving the fig. They have no wings and no survival skills; but they already passed on their genes, so I guess evolutionarily speaking, they’re set.

Some ficus species have only ‘female’ trees, with figs like the ones I just described (pollen and seed producing flowers in the same fig). Others have separate ‘male’ trees and ‘female’ trees. The ‘male’ figs in this case have both male and female flowers, but all the female flowers are devoted to incubating wasps. These figs only produce pollen and wasps. No seeds. Female wasps that emerge from ‘male’ figs must then find a ‘female’ fig to pollinate. But the ‘female’ figs only have flowers with long styles, so the wasp can’t lay her eggs in them. All seeds, no wasps. Female trees are sort of a dead-end for the wasps, but the male trees act as wasp nurseries, continuously providing new pollinators.

So what was this paper about again?

Oh, yeah, sorry. The paper. Figs aren’t just incubators for friendly pollinating fig wasps, they also become home to parasitic freeloader wasps. These non-pollinators lay their eggs in the galls formed by pollinating fig wasps, killing the little fig wasp larva inside and, sometimes, the fig itself. They’re bad for both pollinating wasps and figs, because a threat to the fig wasp is a threat to the fig tree’s reproduction. The authors of the paper wanted to know if male and female fig wasps (the good kind) are attacked equally by enemy wasps.

Non-pollinating fig wasps (or NPFWs) have really long ovipositors, unlike the pollinating fig wasps. They never even have to go inside the fig. Instead, they pierce through the outside and lay their eggs inside the galls made by pollinators. So it stands to reason that they would mostly harm baby wasps that are developing inside flowers closer to the periphery. These are easiest to reach from the outside.

The researchers studied a particular ficus tree in China, F. hirta, that has separate male and female trees. To collect data on the interactions between pollinating fig wasps and NPFWs, the researchers went out into the field to collect male figs with wasps developing inside. They then determined the ratio of male to female fig wasps, the locations of their galls inside the fig, and the location of galls that were invaded by NPFWs. They inspected a total of 792 galled ovules.

Here’s the results:

Figure 6 of Yu & Compton, via PLoS ONE. Galled ovules with larger ovary positions (X-axis) were closer to the center of the fig.

The enemy NPFWs were very common in flowers whose ovaries were closest to the periphery, and rare in ovaries closest to the center. There were always fewer males than females, regardless of position, but that’s just because there are so few males to begin with. In the center-most flower ovaries, the ratio of female to male wasps gets smaller. Mothers are putting the majority of their sons further away from the enemy’s reach.

But how do they do this?

The authors found that there was not a strong correlation between the distance of flower ovaries from the periphery before and after galling. Laying an egg inside a flower causes its ovary and pedicel to grow rapidly, effectively moving it further from the outer edge of the fig. There was a lot of variation in how far away galling moved individual wasp-incubating ovaries. One suggestion put forward by the authors is that maybe mother wasps put more of their gall-inducing chemicals into the first eggs laid (which are usually male) so that they will end up closer to the center.

Regardless of how it happens, having males protected in the center of the fig means that mom has to devote less eggs to producing boys. After all, you only need to have one that makes it all the way to the end. And after he’s done his job, the females can leave the nest and start the whole fig-and-wasp sex story over again.

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Reference:

Yu, H., & Compton, S. (2012). Moving Your Sons to Safety: Galls Containing Male Fig Wasps Expand into the Centre of Figs, Away From Enemies PLoS ONE, 7 (1) DOI: 10.1371/journal.pone.0030833


Filed under: Insect reproduction, Plant sex! Tagged: ficus, fig wasps, interspecies sex, parasitism, pollinator, Scientific literature

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