A Sad Pony Mathematician's blog: Nematode matricide, evolution of ageing, and offspring-mother conflicts

Let's start with one death. Pristionchus pacificus eating a Caenorhabditis elegans.

Pristionchus pacificus is a nematode that can eat many kinds of foods. In this video, it uses a small tooth to puncture the cuticle of its prey, then sucks in the contents.

The Celens (imma call C elegans that) come in two sexes: male and herm. Herms contain only about 300 sperm cells, after using them all, the herm cannot fertilize more eggs, unless it gathers more from mating with a male. Males cannot reproduce on their own and must mate with a herm to produce offsprings.

Celen sex videos can be found on Youtube. A parody is here: Fifty Shades of Worm International Worm Meeting 2015.

Sometimes, fertilized eggs are not laid by the herm, and instead develops inside the herm, and eventually eat the herm within and burst out. This is called "bag of worms" or "endotokia matricida" or "intra-uterine hatching". The process is called "worm bagging" or just "bagging".

The larvas first develop inside the uterus, then burst out of the uterus and grow in the mother's body, until the intestines of the mother breaks. The bacteria inside the intestines provide the larvas with more nutrients, and the larvas grow further, usually moving towards the head of the mother. Maternal death follows, and the larvas emerge from the mother's corpse soon afterwards.

From On Endotokia Matricida and Intra-Uterine Development and Hatching in Nematodes, (Michel Luc et al, 1979):

in some cases eggs developed into larvae which hatched directly within the uterus of the mother; these larvae progressively destroy the body contents of the female and finally reach the exterior through the anterior end or by breaking the cuticle. It is a form of ovovivipary - a matricidal one.

I found a few videos on Youtube that are of good quality.

There's also a cool proprietary video I don't know how to embed. It's titled "Young Worms Inside Female Turbatrix Aceti".

Endotokia matricida is observed in many kinds of nematodes. It was described quite early, in (L. G. Seurat, 1920), Histoire watidrelle des Nématodes de la Berbérie. Première partie: morphologie, développement, éthologie et affinités. Here, Seurat is talking about Heterodera schachtii:

Under normal conditions, eggs , or embryos are expelled through the vulva, but it is not uncommon to observe, especially at the end of summer, that the peripheral tissues of the female are modified so that the whole body is transformed into a brown cyst, designed to protect eggs during the unfavorable season. When this period is over, its wall swells, softens and allows escape of eggs and larvae. As is the case with normal females each of these brown cysts contains 300-400 eggs.

Bagging is not always lethal to the mother, and even if it is, it doesn't hurt the mother's reproductive success. From Bacterium-Induced Internal Egg Hatching Frequency Is Predictive of Life Span in Caenorhabditis elegans Populations, (Thomas Mosser et al, 2011):

However, it is not necessarily lethal to worms. Some worm bags expulse internally hatched larvae and live as long as some non-worm bag individuals... Internally hatched worms survived as well as or better than externally hatched worms. Thus, internal hatching does not negatively impact brood size or offspring survival.

This indicates that it's not a bug, but a feature.

Why tho

According to Facultative Vivipary is a Life-History Trait in Caenorhabditis elegans, (Jianjun Chen, 2004), this is a strategy for Celen herms to increase the chance of offspring survival under stressful situations:

When starved, Caenorhabditis elegans adults retain progeny internally which then consume the parent body contents, and some of those larvae use the resources to reach the resistant, long-lived dauer stage. If starved under similarly extreme conditions, larvae from eggs laid outside of the body are unable to develop into dauers.

What's a "dauer"? When the environment is stressful, a developing nematode can, instead of maturing, turn into a dauer larva, which uses less energy and can lie almost sleeping for months, waiting for better times.

So, the experiment showed that under starvation, larvas that hatched from eggs outside of their mothers can't eat their mothers, and could not even reach the dauer stage. Larvas that ate their mothers developed into dauer stage and could wait for better times.

The ideas in this paper were in fact based on a slightly earlier paper, Why Caenorhabditis elegans adults sacrifice their bodies to progeny, (Jianjun Chen et al, 2003):

Hermaphrodites added to a buffered solution without E. coli essentially stop laying eggs immediately (although some eggs are released later), and the embryos within such hermaphrodites continue to develop and hatch within their parent. Matricidal hatch is induced when population densities are high, nutrient levels are low, or when C. elegans is grown in liquid culture...

As the C. elegans dauer can survive starvation and other stresses that normal juvenile stages cannot, the production of even a single dauer under conditions lethal to other juvenile stages represents a substantial fitness gain to the parent.

Interestingly enough, bagging is survivable if the stress is short:

... bagging is apparently reversible if the stress is removed before the adult has sustained lethal internal damage due to larval movement.

How about the males? Or, why do most creatures get old?

We've been only talking about the herms. How about the males? Male nematodes don't have egg cells in their bodies, only sperm cells, so it's impossible for them to be eaten by babies.

Unlike a herm, who can reproduce both by self-fertilization and mating with a male, a male nematode's only method of reproduction is to mate with a herm. This turns out to allow a male to live longer by 10-20%.

There is an evolutionary reason for this difference in aging, or indeed, for ageing in general. As proposed by (George Williams, 1957), in Pleiotropy, natural selection, and the evolution of senescence, ageing evolved not because long life is hard, but because it's unnecessary:

It is remarkable that after a seemingly miraculous feat of morphogenesis, a complex metazoan should be unable to perform the much simpler task of merely maintaining what is already formed...

To explain how ageing could have evolved, then, Williams proposed the pleiotropy theory: There are some genes that code for traits that are healthy early in life, but unhealthy later in life. It's better to live faster and die younger if it helps you get more offsprings.

The pleiotropy theory of ageing has good empirical support. A recent review is Is antagonistic pleiotropy ubiquitous in aging biology?, (Steven N Austad et al, 2018).

Applied to male nematodes, this explains why they live longer than herms and females.

Aging is not a directly selected trait, but rather evolves as the result of a decreased force of natural selection at older ages. The latter occurs because mortality resulting from extrinsic hazards leads to progressive rarity of members of increasingly older age groups... The evolutionary theory also provides a potential explanation for sex differences in the rate of aging. As proposed by G. C. Williams: ‘Where there is a sex difference, the sex with the higher mortality rate and lesser rate of increase in fecundity should undergo the more rapid senescence’.

Human readers would be interested to know that this is the opposite in humans, though the reason is unclear. See Why women live longer than men: Sex differences in longevity, (Steven N.Austad, 2006).

Historically, women have lived longer than men in almost every country in the world... For virtually all the primary causes of death and at virtually all ages, mortality rates are higher for men. Women do not live longer than men because they age more slowly, but because they are more robust at every age. Paradoxically, although women have lower mortality rates they have higher overall rates of physical illness than do men. Several hypotheses have been proposed for sex differences in longevity... At present, none of these hypotheses are strongly supported...

Offspring-mother conflict in a larger context

Bagging is just an extreme example of a general rule: Good offsprings matter more than good parents.

A report from University of Southern California shows that

When an organism is exposed to external stresses such as famine, gene SKN-1 is activated. In addition to stress resistance, activation of SKN-1 also drives the reallocation of fats from the organism's body cells to its reproductive system. Once there, the fats fuel the development of egg cells, making successful reproduction easier; however, the animal itself faces a higher likelihood of a shortened lifespan.

or in jargon, from Omega-3 and -6 fatty acids allocate somatic and germline lipids to ensure fitness during nutrient and oxidative stress in Caenorhabditis elegans, (Dana A. Lynn et al, 2015):

We identify a lipid homeostasis pathway that regulates the mobilization of lipids from the soma to the germline, which supports fecundity but at the cost of survival in nutrient-poor and oxidative stress environments... Our results describe a mechanism for resource reallocation within intact animals that influences reproductive fitness at the cost of somatic resilience.

Have a few more pictures: