Males Need Not Apply
Males Need Not Apply
These female insects give birth to generation after generation of all-female offspring. Until autumn, when they also produce males — a remarkable case of reproductive autonomy.
IN THE DRAMA of courtship and copulation, it’s no secret that females sometimes go to great lengths to repel the unwelcome advances of males, even among insects.
A female butterfly, for example, flattens her wings and points the tail-end of her body skyward (as if she’s flipping him off).
Some praying mantis females on occasion decapitate and eat males, even during mating.
But female woolly aphids have a more radical strategy: most of the year they have no need for males whatsoever, and give birth on their own to generation after generation of little aphid offspring, all of which are female.
Most of us live unaware in the midst of this remarkable insect performance. That is unless you happen to be noticing tiny bits of bluish fuzz now drifting on the winds of autumn. Not fluffy plant seeds, the fuzzy bits are woolly aphids out for their fall fling. This is their story of female sexual autonomy.
Uncharismatic and most of the time wingless, aphids are better known as plant and crop pests than as icons of sexual innovation. Here in the northeastern U.S., I often find them gathered as masses on Speckled Alder (Alnus incana), sucking liquids and covered with a protective waxy white quilt resembling cotton or wool.
There on the leaves or bark, the aphids defy the standard insect life cycle, which ordinarily goes like this: male meets female, they mate, and she lays eggs, from which larvae hatch and grow in stages to become male or female adults.
From aphid eggs, however, only females will hatch. They develop and grow (by sucking leafy liquids) to a point at which they themselves, without males, produce a new generation of female offspring. But not by laying eggs. The females instead give birth to live young. These “mini-me” “mini-she” aphid children grow and in turn give birth to many successive generations of live females. It is reproduction by means of parthenogenesis (from the Greek virgin birth) and it is viviparous (birth of live progeny).
This all-female reproduction happens from spring into fall, during which aphid numbers can increase dramatically owing to the females’ fecundity and an abundance of leafy plant food for their young. And it all happens without any males on the scene.
Until now.
As the days grow shorter, female aphids relent from their cycles of parthenogenesis and give birth to females and to males. This sets up a change from asexual (or clonal) reproduction (the mini-shes) to sexual reproduction (males and females ready to go at it in autumn). This kind of reproductive switching is unusual — and yet illustrates a remarkable phenomenon in nature.
Just One Word: Plasticity
Plenty of organisms can change their appearance or behavior — in a regular and predictable way — from one generation to the next. Insects exemplify this because they often produce multiple generations in a given year. Mustard White (Pieris oleracea) butterflies, for example, have distinct dark veins on the underside of their hindwings in springtime, but their offspring flying in summer show faint veins. Same butterfly species, different appearance by season.
Similarly, the Monarch (Danaus plexippus) butterflies many of us see flying in spring live for a month or so, as do their offspring in summertime. But the generation of Monarchs flying in fall do not live for a month — they live for about eight months and they migrate to Mexico. Same species, still a Monarch, but hugely different “life ambitions” according to season.
All sorts of environmental conditions can drive this kind of change in appearance or behavior in animals: temperature, day length, diet, the presence of predators, or who knows what. The point is that species aren’t as fixed in their ways as we might think. They can be shaped or molded, like soft plastic, depending on what they encounter in their environments. We call this variability phenotypic plasticity. It’s not that unusual.
What is unusual, however, is an animal changing the way it goes about reproduction. In the case of aphids, the plasticity isn’t about appearance (like the veins on a butterfly) or even about behavior (like a migratory Monarch). It’s about something far more fundamental: a female’s means of developing offspring — reproductive plasticity. The seasonal switching from asexuality to sexuality (now featuring males) is not unique to aphids, but it’s rare. More than anything, it might have you rethinking your notion of insect intelligence.
An Aphid’s Tiny, Powerful Brain
Throughout spring and summer, sisterhoods of aphids have been producing even more sisterhoods of aphids. But something now triggers them to bring males into the world as well. Although the finer points of this are still subject to debate (and I’m generalizing here by necessity), it appears that plenty of aphid species can decipher three environmental cues:
Photoperiod — Aphids seem to have the ability to measure day length. Shorter days of autumn trigger female aphids to overhaul their means of reproduction to now include giving birth to males.
A Day Counter — Aphids might also keep a count of those shorter days — perhaps needing to record about 10 or more in a row past a crucial trigger day-length — in order to be certain of the seasonal trend.
Temperature — Warmer weather might override the short-day trigger, however, causing female aphids to delay the point at which they give birth to males.
In any event, a male aphid flying or walking around this autumn can quite likely thank his mother for her ability to size up the world and keep track of things. (Sound familiar?) Basically, in their reproductive biology and self-interest, female aphids seem to be running two evolutionary gambits:
First, the asexual reproduction is a numbers game — females (without interference or sperm from males) producing more and more female offspring while food is abundant in spring and summer. It’s good for survival, a hedge against predation.
Second, in their autumnal switch to sexual reproduction, females probably bring males into the world for at least two reasons. One is that the males add genetic diversity to aphid offspring, which is good for the species. (So, to be clear, males aren’t entirely superfluous in aphid biology.) Also, after they mate with males, the females, rather than producing live young, go on to lay eggs this time around, which can remain viable through winter (and from which in spring only females will hatch to resume the reproductive cycles of sisterhood).
The Feminine Mystique
Although I’m out on a limb here, it seems that aphid reproductive biology is in many respects ruled by females. (Maybe that’s one reason aphids do not wage senseless wars upon one another.)
Among many animal groups females bear a disproportionate share of the burden of procreation — risks ranging from harassment by males to exhaustion to death. So it should come as no surprise that females, even among lowly or prosaic insects, might therefore seek some sovereignty in the arena of reproduction. The stakes are just so much higher for females.
What we seem to be seeing among aphids is not simply a female mixing her genes with those of a male in order to gain fitness for their young in the struggle for existence, but rather a female also taking it upon herself to radically switch her reproductive strategy so that her genome gains strength in numbers among her offspring. Call this whatever you’d like — self-preservation, autonomy, even feminism. It constitutes a fascinating line of wildlife research (about which I will continue to write into the future).
But for now, at long last, I offer you an intimate encounter with this drama — fuzzy aphids now in flight. Depending on the species, males or females (or both) of the autumn aphid generation can have wings. That includes what we generally call wooly aphids resembling tiny bits of bluish-white fuzz (and easily passed off as floating plant material). They’re not much bigger than grains of rice.
I’ve seen them called “fairyflies” (which is actually a more proper common name for a group of incredibly tiny wasps in the family Mymaridae). My partner Ruth coined the endearing term “Blue Fuzzy-Butts” — for their bluish bodies with wispy growths of woolly fuzz, which presumably makes the aphids less palatable to predators.
By any name, they’re on the wing now near many of us in North America and Europe. Find them often floating in the vicinity of apple trees, elms and alders and their relatives. Find them in gardens and even in cities.
When you do, reach out so that they might alight on your hand. Say hello. Make a wish. Whatever. Then send them on their way. After all, now is the only time of year that female and male aphids have vital business together.
Postscripts and Caveats
Somewhere around 5,000 different species of aphid inhabit the world, exhibiting any number of variations on this theme; so my account above generalizes these cycles in some respects.
Some aphid species switch their preferred plant hosts during the year. To do this the sisterhood produces an interim generation of winged females that fly off to the new plant.
When they hatch from eggs, aphid females do undergo larval development (three or four instars) before they begin bearing live young (viviparous parthenogenesis).
And I haven’t even mentioned the partnership between aphids and ants.
Many of the Blue Fuzzy-Butts are woolly aphids in the tribe Eriosomatini, probably in the genera Tetraneura, Eriosoma and Prociphilus (depending on location and plant hosts).
References
I knew little of aphid reproduction until I read these:
“Shifting from clonal to sexual reproduction in aphids: physiological and developmental aspects” by Gaël Le Trionnaire, Jim Hardie, Stéphanie Jaubert-Possamai, Jean-Christophe Simon and Denis Tagu. Biol. Cell. (2008) 100, 441–451
“Aphid polyphenisms: trans-generational developmental regulation through viviparity” by Kota Ogawa and Toru Miura. Frontiers in Physiology (2014) Vol. 5.
“Evolutionary and functional insights into reproductive strategies of aphids” by Jean-Christophe Simon, Solenn Stoeckel, Denis Tagu. C. R. Biologies (2010) 333 488–496.
“New data on the aphid (Hemiptera, Aphididae) fauna of New Caledonia: some new biosecurity threats in a biodiversity” by Christian Mille, Hervé Jourdan, Sylvie Cazères, Eric Maw, and Robert Foottit. ZooKeys (2020) 943, 53–89.
“Cyclical Parthenogenesis and Viviparity in Aphids as Evolutionary Novelties” by Gregory K. Davis. J. Exp. Zool. (Mol. Dev. Evol.) (2012) 318B:448–459.
The brilliant entomologist Charley Eiseman covers woolly aphids, among many other wonders, at his phenomenal site BugTracks.
This is alluded to indirectly in your essay, but a major advantage of parthenogenetic production of females is that it more or less doubles the population growth rate. Only females can contribute to the future population because only females can produce more aphids. Males are a waste in this context. Because aphids are everybody's favorite lunch, this extreme population growth rate, in effect, outruns mortality by predation (think aphid lions, parasitic wasps, ants, fly larvae, etc).
I don't know if woolly aphids do this, but in some aphid species, crowding induces the development of wings in some of the parthenogenetic offspring. These winged females then fly off to found new colonies.
As you showed for woolly aphids, aphids in general are really fantastic creatures, unendingly interesting and surprising.
I adore this essay. You have such a gift for making science and life in general both fascinating and discernible. The first time I ever saw these in large numbers was the first Covid year when I took the dog for her evening walk. They came up as a topic of "WTF are these?" during my recent Master Naturalist course, at which point I was introduced to them as "you mean those tiny little insects with blue tutus?" So now they're also Tiny Tutu Bugs in my neighborhood. Assuming they're the same beings. (The only thing I regret from that course is the implantation of the ever-present question "But is that a TRUE BUG?")
Unrelated: I seeded milkweed two weeks ago! Spent a day clearing thistles and quack grass out from all along the raspberry bed and put them in there. The sunflowers did well there this year, so I have hopes. 🤞🧡🌻(why no milkweed emoji?)