Save some of that sperm for later

Long-jawed Orb Weaver (Nephila senegalensis).

Nephila senegalensis female. Image via Flickr.

In spiders, there are many species where the males only get one chance to pass on their genes. They stop making sperm as soon as they become adults, and after one sexual encounter, their sperm are all used up. In the great game of evolution, this isn’t the best strategy. They’ve quite literally put all their eggs in one basket.

Once monogyny–a system in which each male mates with only 1 female–has evolved, it’s thought to be an evolutionary dead-end. That is, any species that evolves from a monogynous ancestor should also be monogynous. The extreme adaptations that males develop to deal with this system may be impossible to come back from.

But there is hope for these poor males! A new study on an African spider species, the banded-legged golden-orb spider (Nephila senegalensis), found that even though this species’ close relatives are monogynous, its males have developed a unique strategy to stretch their sperm supply: splitting up what little they have between many females. The findings were published by Jutta Schneider and Peter Michalik in the journal BMC Evolutionary Biology. You can read the full article here.

Testes from N. senegalensis males. The subadult testes are from males that aren’t fully mature. These testes are larger and produce sperm. After 1 day of adulthood, though, they’ve already begun to shrivel up. Image adapted from Figure 1 of the paper.

Like its close relatives (and probably its ancestors), male banded-legged spiders don’t make sperm anymore once they become adults. Spiders have a special way of mating: the males will spin a small, special web that they then ejaculate on. For the monogynous species, and the banded-legged spiders, this only happens once and uses all the sperm from the male. Males then dip their pedipalps (specialized legs) into the sperm-containing fluid and load up the syringe-like structures on their ‘palps that they insert into the female during sex.

I mentioned extreme adaptations that males develop to deal with monogyny. How extreme, you ask? Would you count self-inflicted genital mutilation as extreme? Monogynous males have a vested interest in keeping the one female they mate with from mating with anyone else. After all, if she decides to use some other guy’s sperm to fertilize her eggs, he’s out of the evolutionary race.

One way to keep a female from mating again is to physically plug her so no one else can get any sperm in. What can a male use as a plug? How about that pedipalp he just inserted to deliver his last load of sperm? This kind of “terminal investment strategy” has evolved many times in monogynous males.

An extreme example is Tidarren argo. Males of this species will only ever get a chance to mate with 1 female and he will only be able to use 1 of his pedipalps. Because the pedipalp of this male is 20% of his body mass, it’s more efficient if he just cuts one off at the beginning. Then, if he’s “lucky” enough to mate with a female, he will sacrifice himself as a meal to her during sex. When she eats him, his pedipalp remains in copula to see the job through to the end. Other species may not become food, but will amputate their pedipalps after sex (they’re no good anymore, right?), a practice known as the “eunuch phenomenon”.

Genital mutilation doesn’t always come along with monogyny. The genus Nephila has nearly lost it entirely (except for one species). The hero of our story, N. senegalensis, does not have genital mutilation, and whether it is strictly monogynous wasn’t clear before this study was done.

The researchers had three questions:

1) Does sperm production stop at maturity? (Answer: yes).

2) Can males fertilize the eggs of more than 1 virgin female?

3) Do females in this species mate with many males (which would increase male-male competition)?

To answer question #2, they mated males to 5-9 virgin females, only letting them use 1 pedipalp for the mating. What they observed was that males were able to fertilize the eggs of the first 4 females they mated to, but after that they were sterile. It’s interesting that even though all their sperm was used up in the first 4 matings, the males still happily copulated with more females.

Since the males had only charged up their pedipalps once, this suggested that they were actually able to split up each sperm load into 2 matings. By being frugal with their sperm, they doubled the number of females they could inseminate!

Next, the researchers wanted to know whether males always split up the sperm load in a single pedipalp into 2 matings, or if they could be induced to change their strategy. To test this, they made the males into half-eunuchs by amputating one of their pedipalps (sad face!). These males still went about their business as normal, splitting up the sperm load into 2 matings. One male was actually able to stretch it out to 3 matings, but none of them succeeded in fertilizing eggs with 4 females. (One poor male “could not be motivated to copulate with more than 2 females.” I guess he knew the jig was up).

Long-jawed Orb Weaver (Nephila senegalensis)

You can see the tiny male above the female in this picture. Image via Flickr.

Some of the males in both experiments only fertilized the eggs of 1 female. All of the copulations were timed, and it turned out that the length of time a male mated predicted whether he would have enough sperm left to inseminate another female. Males who only inseminated 1 female mated with that female twice as long as their more frugal counterparts. It seems that a little self-control is needed on the part of the male to maximize his sperm investment.

What about question #3, female polygamy? The researchers gave females up to 13 males to mate with, in succession. It turns out that the only thing limiting the number of times a female will mate is how many males there are available. These ladies weren’t choosy. They accepted pretty much any male (spermless or not).

The most interesting thing about this experiment was how they had to do it to keep the males safe. Before the mating trial, females were given a fly to munch on. This way, she wouldn’t be too tempted to eat her suitor. This worked in all but one case.

What does all this tell us about the evolution of sex? It shows that a species can bounce back from monogyny, if the conditions are right. In this case, it only took the males changing the way they invested their limited sperm to double the number of potential mates, compared to their relatives. This is presumably much easier than changing their whole development to keep sperm production going past adulthood. We’ll have to check back in a few million years to see if they get that back, too.

But a lot of questions remain unanswered. Do males actually mate with more than one female in the wild? Or do they just mate with the same female over and over, in order to win at sperm competition (remember, these females are promiscuous). Or might they change their strategies, depending on the situation? More field studies are needed to answer these questions.

Schneider JM, & Michalik P (2011). One-shot genitalia are not an evolutionary dead end – Regained male polygamy in a sperm limited spider species. BMC evolutionary biology, 11 (1) PMID: 21740561

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