Having sex with another species

Looking for a sexual partner outside your species is not very common, but that is what the males of a type of spider mite do. Even more, a recent work¹ suggests that this kinky behaviour could have been key to colonization of new environments.

Tetranychus evansi is a species of red spider mite originally from Brazil that has recently spread to Africa, Southern Europe and East Asia. Spider mites receive their name from their ability to spin webs around the leaves of the plants they invade. Underneath these webs, groups of individuals live and reproduce, feeding themselves on the leaves by puncturing them and sucking out their cellular content, eventually causing defoliation. Since their life cycle is short (13.5 days) and each female can lay up to 200 eggs, they can spread rapidly and cause severe damage to crops, specially tomato plantations.

During its expansion from South America, T. evansi came across a close relative, Tetranychus urticae, which is the most common form of red spider mite in the Old Continent, and that shares with T. evansi a taste for tomato plants. It is not clear what selective advantage allowed T. evansi to colonize a territory in which a related species was already thriving. But considering that they are phylogenetically very close, a group of researchers from the University of Amsterdam decided to test an interesting hypothesis: reproductive interference.

Going xenophilic

The boundaries between species are somewhat blurred, but most biologists would agree that the inability to produce fertile offspring is a reliable sign that two groups belong to different species. As speciation occurs, a number of mechanisms evolve in parallel to ensure reproductive isolation. These barriers start as molecular (i.e. the sperm from one species is unable to recognize and fecundate the egg from another) and, as the two species become more divergent, end up being physical (the reasons why mice and cows can’t cross are obviously beyond sperm incompatibility). In some cases, closely related species can still copulate and give birth to sterile hybrids like the hinny, which is the offspring of a male horse and a female donkey.

T. evansi and T. urticae are so similar that they are often misclassified by entomologists. Their divergence has taken place recently, evolutionarily speaking. Since natural selection hasn’t had time to shape each group, it is not uncommon for these closely related species that males mate females from the other kind, allegedly because they can’t tell them apart from their own. Considering the energetic cost of reproduction and that the offspring of crosses between different species is not viable (if there’s any offspring at all), this reproductive interference often has negative consequences for at least one of them, making the interaction between the two species much more complex – and interesting.

To study reproductive interference in these mites, the researchers first evaluated if heterospecific crosses could take place. To do this, they performed crossing experiments putting together three males and a female in tomato leaf discs and recorded them with a camera. While T. evansi males never missed a chance to copulate (whether with a female from its own species or with a T. urticae female), T. urticae males chose not to copulate with a T. evansi female about 20% of the times but were always willing to do it with one of their own kind. Also, it was noted that interspecific copulations lasted considerably less – probably because it feels a bit awkward to have sex with someone from a different species.

The next experiment was designed to answer a more interesting question: if males could choose between a female from their own species or from the other one, which would they choose? T. urticae, the local kind, had already made clear in the previous experiment that it wasn’t so fond for T. evansi females. When given a chance to choose, it preferred conspecific females in more than 80% of the cases. However, T. evansi turned out to be quirkier and repeatedly chose T. urticae females over those from its own species.

Like other insects, such as bees and ants, spider mites are haplo-diploid, which means that females carry two copies of DNA in each cell while males carry only one. When males and females mate, the egg is fertilized by sperm and gives rise to a female; if the eggs go unfertilized, males are born. After the mating experiment, the researchers observed that females were only born when both male and female were from the same species, indicating that though interspecific mating is possible, eggs can only be fertilized by sperm from a conspecific male.

So apparently, males from the invader mite prefer local females over those from their own species. However, this mating does not produce fertile eggs and hence no females in the offspring, decreasing the overall fitness of the local species. The authors hypothesized that this could have been one of the strategies that allowed T. evansi to outcompete T. urticae. To test this idea they evaluated how the two species interacted during the infestation of a tomato plant in the lab. The experimental design included two settings, termed mild and strong reproductive interference. In both of them eight individuals, two from each species and sex, were introduced in the same plant and the number of total females was followed by four weeks. The difference between the two conditions was that in the mild one the founder females had already mated with a conspecific male, avoiding reproductive interference during the first generation, whereas in the strong condition all founder females were virgin. The results showed that while in the mild condition T. urticae outgrew T. evansi, this asset was lost in the situation of strong reproductive interference. This suggests that reproductive interference could be an important factor in the interaction between these two species.

Of course, the real picture is probably far more complex and includes many other factors. For example, it is known that T. envasi can block the stress response of the tomato plants, which facilitates the colonization for both species. (In the aforementioned experiment a mutant plant without that specific stress response was used to minimize this effect). Also, the way how each species interacts with their natural predators is definitely an important element in the equation. But perhaps uncovering the licentious lifestyle of this pest might help to find a way of keeping it away from the crops. After all, our perversions are also our weaknesses.