By Yael Lubin
Maternal care can be costly. In fact, prolonged maternal care can sometimes cause a mother to delay or even forego producing additional young.
An extreme case of costly reproduction occurs in the spider Stegodyphus lineatus (in the Old World family Eresidae), where the mother has only a single small clutch of young during her entire lifetime. The young require the mother’s help to exit their silk eggsac, and they are totally helpless when they emerge. Without the mother’s care, they would die.
The mother feeds her young by regurgitating liquid food. Then after two weeks or so, the young reward her efforts by killing and completely consuming her, leaving an empty exoskeleton.
This process, known as matriphagy, is suicidal maternal care, because the mother makes no attempt to escape her fate.
Matriphagy was first described in the last century by the German arachnologist Ernst Kullmann, and an interesting observation was made by his student S. Nawabi, who suggested that the mother spider might actually digest her own tissues to feed her young.
This piqued the curiosity of Dr. Mor Salomon, a postdoctoral fellow in entomology at the Robert H. Smith Faculty of Agriculture, Food & Environment, the Hebrew University of Jerusalem, who had studied maternal care in Stegodyphus for her doctoral research. She wondered whether females do indeed digest their own bodies, and if so, when in the reproductive cycle does the process begin? Which tissues are digested, and what changes occur inside the female during this process? The answers to these questions appear in an article in the Journal of Arachnology.
Stegodyphus lineatus spiders occur in the semi-arid regions of Israel and other parts of the Mediterranean basin, and throughout the Near East and in Asia Minor. Mor Salomon took adult female Stegodyphus lineatus spiders at five different stages of their reproductive cycle — virgin females, mated females, females that had laid eggs, young that were released from the eggsac and fed by their mothers, and the young just prior to committing matriphagy. She anesthetized the spiders, fixed them in formalin, and embedded them in resin in preparation for histological work. Serial sections were then cut through the abdomen and stained with chemicals to detect proteins and nucleic acids. This enabled Salomon and her colleagues to distinguish various types of tissues and cell nuclei.
Spiders have a remarkable digestive system. Their midgut tubes have a large number of blind extensions that fill most of their abdomen. In these extensions, the midgut diverticula lobes, that digestion of nutrients takes place. Digested nutrients are then transferred into the lumen between the lobes and into intermediate tissues for storage and distribution to the body tissues.
In their study, Mor Salomon and her colleagues confirmed Nawabi’s suspicion that in both virgin and mated adult females, cells of the diverticula lobes are filled with lipid droplets and vacuoles (intracellular “pockets”) containing digested nutrients.
However, after egg-laying, these diverticula lobes begin to degenerate. Cell walls become blurred, and the vacuoles and lipid droplets begin to disappear. This degeneration of the diverticula and the surrounding tissues intensifies after the young emerge from the eggsac and during the regurgitation stage, when pockets of liquid appear in the abdomen. Just before matriphagy occurs, much of the spider’s abdomen is liquefied. Interestingly, the ovaries, the heart, and surrounding tissues are the last organs to degenerate.
When the young hatch, Stegodyphus lineatus females stop repairing their sticky capture webs since they will no longer feed on prey. The liquid that is regurgitated to the young is derived, therefore, only from the digested nutrients stored in the midgut diverticula and other tissues in the abdomen. These observations suggest that maternal care is a one-way street for these spiders, and once the process of tissue disintegration begins, the female’s only option is to continue on to matriphagy.
Nevertheless, this extreme reproductive system seems to retain a degree of plasticity. In an earlier study on the same species, Jutta Schneider and colleagues showed that if the young are removed from a female’s nest a few days before matriphagy, the female can still produce a replacement eggsac. Salomon’s results support this, given that the ovaries were one of the last organs remaining intact in the female’s abdomen. This may be an important backup plan, since offspring in the nest are often killed by predators like parasitic wasps and ants. In such a situation, the female is still able to produce another clutch.
All species of Stegodyphus observed so far have suicidal maternal care, and we presume that similar changes occur in their female digestive systems during the maternal-care stage. Interesting questions arise, however, regarding three species of Stegodyphus that are social and have cooperative brood care.
In her PhD studies, Mor Salomon showed that large immature females — and mature females that fail to reproduce — can act as helpers at the nest. These helpers regurgitate food and are eventually killed and eaten by the young of other females in the colony. She also showed that the help provided greatly improves the chances of survival of these young.
Do these helpers undergo the same processes of tissue degeneration? If so, what are the cues that initiate tissue degeneration, given that these females do not reproduce themselves? Are these helpers locked into suicidal support?
Some of these questions are currently being investigated in the laboratory of Professor Gabriele Uhl at the University of Greifswald in Germany.
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Yael Lubin is a professor emerita at the Mitrani Department of Desert Ecology, the Jacob Blaustein Institutes for Desert Research at Ben-Gurion University. Her research focuses on behavioral and ecological questions about spiders, including the evolution of sociality, sexual behavior, and spiders in agroecosystems.