Virgins Birthing

Nature-Nurture-Noise (5)

Most animals reproduce sexually, that is, through the union of a female egg (ovum) and male sperm. The fertilized egg, called a zygote, then begins to divide in the first stages of development, called embryogenesis. More than a few animals, however, eschew sex at least some of the time. In asexual reproduction the zygote is an unfertilized egg, hence the name parthenogenesis, which is Greek for virgin birth. The Amazon mollies discussed in the previous post in this series (Nature-Nurture-Noise 4 ), are not truly parthenogenic, as conception is far from immaculate. In this chapter we will consider truly parthenogenic species for which sperm—and hence males—are completely inessential.

Sexual reproduction is the ancestral condition for all animal species, from sponges to worms to mammals. But a diverse array of animal species, have, secondarily, evolved some capacity for parthenogenesis, especially invertebrate species, including a variety of insects and crustaceans.

There are several forms of parthenogenesis, all of which require only the female gamete or ova (unfertilized egg) to initiate development. Only one of these forms of parthenogenesis generates true clones. Clonal parthenogenesis is the most common form of parthenogenesis, however, and this is the kind of parthenogenesis that will concern us here. Like isogenic populations created through careful breeding in the lab, and gynogenic mollies, parthenogens provide ideal subjects for exploring developmental randomness. Let’s first consider a species in which parthenogenesis is a natural part of the life cycle.

Jump or Sit

Aphids are reviled by gardeners and farmers alike. There are more than 5,000 described species. Most specialize on one or a few closely related pant hosts, from which they extract phloem (AKA sap), the nutrient laden liquids that function much like blood in animals; phloem distributes essential biochemicals to distant cells. To this end aphids have evolved specialized mouthparts to pierce and suck, analogous to those of a mosquito. In doing so they impair both the circulation of the phloem and render the plant vulnerable to viral infections.

My own experience with aphids is largely confined to the species that plagues roses (Macrosiphum rosae). Of far more consequence are those species that afflict commercial crops such as potatoes, soybeans, wheat, oats, citrus, and other economically important domestic plants. One species, which vexes both artisanal and commercial food growers, prefers legumes such as peas, broad beans, and alfalfa. Called the pea aphid (Acyrthosiphon pisum), it is much larger than the rose aphid and indeed most other aphid species. Due in part to its economic importance it has become a model organism in biology and has a long history in the lab, where husbandry techniques for this species have been perfected.

All aphid species are parthenogenic to a large degree, some exclusively so. Most, though, are seasonally—or cyclically—parthenogenic, including both the rose and pea aphids.  They are parthenogenic from spring to autumn. As winter approaches, they switch to the sexual mode. Only the female, sexually produced eggs, overwinter. Come spring, these females hatch and begin reproducing genetically identical daughters through parthenogenesis.

Parthenogenesis is key to the explosive population growth of aphids. A single female typically produces 10 to 12 broods of genetically identical female offspring during a season, each of which can begin birthing their own all female offspring in 10-12 days. I say “birthing” because aphids during the earliest stages of development the young or nourished inside the mother and born live, rather than inside an egg. We can be grateful that pea aphids aren’t “telescopers”, which is characteristic of many other aphid species. Telescoping is so-called because the nymphs inside the mother, themselves carry less developed nymphs inside theirs, and sometimes these nymphs in turn harbor even less developed nymphs. Telescoping aphids have an even greater potential for explosive population growth than rose or pea aphids.

Each aphid is genetically identical to both its mother and sisters—a clone, in other words. So, it is noteworthy that there is substantial variation within aphid clones for a variety of traits, including pesticide resistance, susceptibility to fungal parasites and parasitic wasps. Some of this variation can be attributed to environmental effects, some to genetic variation within clones. The latter becomes particularly significant over long time periods, as even clonal aphids have the potential to evolve rapidly—albeit less rapidly than sexual species—through mutations that render clonal populations slightly genetically heterogeneous. As such, to understand clonal variation independent of genetic and environmental effects it is important to look for differences within a single aphid generation under controlled (environmental) conditions.

As all gardeners know, ladybugs are voracious aphid predators. When confronted with a ladybug, some aphids immediately drop to the ground; others, though, sit tight. You might assume that those that drop would have a better chance of survival, but things are not that simple. There are tradeoffs involved. Those that sit, it is true, are more likely to be ladybug fodder. But if they avoid becoming prey they can immediately resume feeding once the ladybug departs. The droppers, though safe from ladybugs, are confronted with an alien, often desiccating environment sans nutritional resources. Lacking wings, it is only with great effort (energy cost) that they can climb back to a food source. Not surprisingly, in genetically varied aphid populations an equilibrium between sitters and droppers evolves, depending, in part, by the number of ladybugs around.

In the experiments conducted by Yang-Li and Shin Chi-Akimoto at Hokkaido University, the aphids whose response to ladybugs was monitored, were raised in isolation under identical controlled conditions. As important, they were all offspring of a single female. Hence, their genetic sameness was guaranteed. Yet, despite both genetic and environmental uniformity

there was still individual variation within broods, in the behavioral propensity to drop or sit tight in the presence of a ladybug. That fateful decision, it seems, was not environmentally nor genetically determined, more like a coin toss. But the coin toss occurs early in development, not upon initial exposure to the ladybug. Once the coin lands the individual aphid is either a jumper or a sitter for life. Chancy developmental processes are of great consequence for pea aphids

Two kinds of eggs

A similar binary “choice” confronts the tiny (0.2-.6 mm) freshwater critter commonly referred to as the water flea, because of its propensity to move in jumps. But water fleas are more closely related to lobsters than aphids; they are crustaceans, not insects. There are a number of water flea species, many in the genus Daphnia, named after Daphne, the water nymph of Greek mythology.

Daphnia are an important element of the ecology of lakes and ponds, near the base of the food chain. Their diet consists of organisms at the very base, such as algae and bacteria. Daphnia are themselves consumed by a wide variety of lake inhabitants, including aquatic insects, larval amphibians (tadpoles) and small fish. Aquarists maintain Daphnia as a food source for fish fry. I used to collect them each spring from ponds in the foothills of the Sierras to that end.

Daphnia, like aphids, alternate—seasonally-- between clonal and sexual reproduction. (What follows concerns Daphnia in the clonal condition.) And like aphids they have become model organisms in biology and have a long history in biological laboratories worldwide, mostly for testing the effects of various pollutants and toxins. But water fleas are also ideal for the study of random developmental variation. For the study described here the trait under investigation is the “choice” of whether to develop eggs that will hatch immediately, or to lay eggs that will undergo diapause, a form of suspended animation, until the next Spring. Those that hatch immediately do so within the brood pouch, to be released within a couple of days into the water. Each brood consists of only one or the other, not mixtures of the two. The two sorts of eggs are easy to distinguish by color and size, clearly visible within the mothers’ transparent bodies.

Dmitry Lajus, of St. Petersburg University, reared genetically identical Daphnia females from a single brood, singly, in identical, carefully controlled environments. He then noted whether their eggs were of the sort that will hatch immediately or enter diapause. As in the aphids, you would expect the genetically identical individuals reared under identical conditions to make the same choice, in this case, the type of egg produced. But like aphids, Daphnia violate these expectations, because of some randomizing developmental process in the mother.