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Male primes female for reproduction - but at a cost

Research has discovered that male worms, through an invisible chemical "essence," prime female worms for reproduction but with the unfortunate side effect of also hastening her aging. The results might lead to human therapies to delay puberty or prolong fertility.

"The male signals trigger the female to 'go for it' — to put more effort into reproduction — but then the body suffers," said Ilya Ruvinsky PhD, of the department of molecular biosciences at Northwestern University's Weinberg College of Arts and Sciences. "There is a fine balance between reproduction and body maintenance, a balance that can be tipped by the male. We now are starting to tease apart this complexity." Published online by the life sciences journal Current Biology, it also will appear in print in the Oct. 24 issue.

The paper: "Sexually antagonistic male signals manipulate germline and soma of C. elegans hermaphrodites," was conducted at the University of Chicago by Ruvinsky and Erin Z. Aprison PhD, both formerly affiliated with the University of Chicago before moving to Northwestern University.

Using the tiny transparent roundworm C. elegans, a well-established model for biomedical research, Ruvinsky and Aprison identified two distinct signals produced by males that affect female reproduction. Females sense the signals and respond by altering their physiology.

Ruvinsky: "We were investigating how animals reproduce under conditions closer to natural environments, other than the cushy life they have in the laboratory. One signal causes an earlier onset of puberty in juvenile females. The other slows down aging of the reproductive system in mature females, keeping them fertile longer. However, it also speeds up aging of the female."

A male animal doesn't even have to be present to cause these changes in a female. A miniscule amount of two male pheromones is enough to affect aging. Pheromone molecules are produced and released into the environment to alter the physiology or behavior of other members of the species.

Although the signals target reproduction, even sterile females – ones without eggs — experience these profound changes.

"Our results regarding puberty onset echo previous findings in mice.

"In mammals, males also produce signals that manipulate the timing of sexual maturation of females. This raises an intriguing possibility that a basic mechanism controlling the rate of sexual development is similar in all animals.

"Because of this universality, our findings may have implications for humans."

Ilya Ruvinsky PhD, Department of Ecology and Evolution, The University of Chicago, and Department of Organismal Biology and Anatomy, The University of Chicago, Chicago, USA.

Fortunately, the research suggests that the effects on sexual maturation, the reproductive system and overall body health can be separated, providing an area for future study. Understanding these basic mechanisms could lead to therapies that delay puberty and prolong fertility in humans as well as combat aging.

Ruvinsky and Aprison used genetics and imaging to characterize female responses to male signals, including prolonged fertility and decreased longevity.

They also demonstrated that steroid hormones, involved in a wide variety of developmental and physiological processes in all animal species, play a key role in converting a male signal into faster sexual maturation in females.

The work was conducted using C. elegans because this simple organism is barely 1,000 cells in total and is easy to grow. It has a short lifespan and offers a tremendous arsenal for experimental manipulation. This laboratory workhorse, affectionately called "the worm," has yielded numerous insights into basic biological phenomena with dramatic implications in human health.

Abstract Highlights
•C. elegans males produce multiple signals that affect hermaphrodite physiology
•Male ascaroside pheromones delay the loss of hermaphrodite germline precursor cells
•Male ascarosides promote somatic aging even in hermaphrodites lacking the germline
•An unknown signal accelerates larval development, specifically the onset of puberty

Males and females pursue different reproductive strategies, which often bring them into conflict—many traits exist that benefit one sex at a cost to another [ 1 ]. Decreased female survival following mating dramatically demonstrates one aspect of this phenomenon [ 2–5 ]. Particularly intriguing is the evidence that secreted compounds can shorten lifespan of members of the opposite sex in Drosophila [ 6 ] and Caenorhabditid nematodes [ 7 ] even without copulation taking place. The purpose of such signals is not clear, however. While it is possible that they could limit subsequent mating with competitors or hasten post-reproductive demise, thus decreasing competition for resources, they are also likely to harm unmated individuals. Why would a system exist that reduces the vigor of potential mates prior to mating? Addressing this question could provide insights into mechanisms and evolution of sexual conflict and reveal sensory inputs that regulate aging. Here, we describe two distinct ways in which Caenorhabditis elegans males cause faster somatic aging of hermaphrodites but also manipulate different aspects of their reproductive physiology. The first, mediated by conserved ascaroside pheromones, delays the loss of germline progenitor cells. The second accelerates development, resulting in faster sexual maturation. These signals promote male reproductive strategy and the effects harmful to hermaphrodites appear to be collateral damage rather than the goal.

Associated articles:

New type of cell death may help neurons regenerate
  Apr 18, 2016
A new type of cell death found in C elegans mimics cell death seen in human neurons, and may lead to regenerative therapies for human neuron injury.

Simple flip of a genetic switch begins aging August 4, 2015
Scientists have pinpointed the start of aging and discovered it is not a slow series of random events. Two Northwestern University scientists have identified a molecular switch in the transparent roundworm C. elegans, that abruptly begins cell aging just as the animal reaches reproductive maturity.

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Sep 26, 2016   Fetal Timeline   Maternal Timeline   News   News Archive   

Caenorhabditis elegans or C. elegans is a roundworm. Above, axons, nerves, are illuminated
in white. Its simplicity does not eliminate it from significant contributions to mammalian research.
Image Credit:
Craig Millman and Yanik Lab MIT



Phospholid by Wikipedia