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Fathered by the dead: Guppies push the extremes of reproduction

Where is my dad, mum? Alice Chaos

All organisms have been evolutionary programmed to spread their genes as far and wide as possible. One way to do that is to produce many offspring, and for that animals have developed some very strange tactics of reproduction.

For instance, the [Antechinus], a tiny marsupial carnivore, has a “live fast and die young” pattern (also known as “big bang reproduction”) in which the males mate for two weeks straight. In the process, they bring themselves to such a state of exhaustion that their immune system fails, and they die. This behaviour may seem like a rather unwise choice, but it seems to work for them …

Agile antechinus. Wikipedia

The Trinidadian guppy has found an even stranger way - by fathering offspring after death. In a recent paper in the journal Proceedings of the Royal Society B, David Reznick of the University of Pennsylvania reports that female Trinidadian guppies (Poecilia reticulata) can store sperm from a male and continue to use it to fertilise eggs for generations even after the male’s demise.

Reznick has been studying Trinidadian guppies for many years. The species exhibits rapid evolutionary responses, making it a great model for answering questions that evolutionary biologists are interested in.

Earlier research showed that female guppies have special adaptations for storing and nourishing sperm after they mate. Lab experiments showed that these females can reproduce long after they have been removed from the presence of males. Also, Trinidadian guppies exhibit a large difference in lifespan between the sexes. Female lifespans can actually stretch over several male generations — they may survive up to two years, in contrast to just three to four months for the males.

All this raises an interesting question: given the sperm storage capabilities of females, and the fact that they outlive males by a wide margin, is it possible that some sperm is technically fertilising eggs and producing offspring after the father himself is dead?

The data for the recent study came from a set of guppies that had recently been introduced to a stretch of the Lower LaLaja tributary in Trinidad’s Northern Mountain Range. The researchers put the guppies in tanks to mate, then released them into a contained tributary. They returned at regular intervals to capture the guppies and collect both demographic information and DNA samples.

When it became apparent that there were more fathers producing offspring than there were reproductive males in the population, the team decided to analyse the demographic and genetic data to answer several questions: whether posthumous reproduction was occurring, and just how common it might be, relative to “traditional” reproduction (that is, fertilisation with the gametes of two living animals). This was a perfect opportunity for such a study, because the animals were already individually marked and had known pedigrees.

Strange sex lives

The results confirmed the researchers’ hypothesis about posthumous reproduction. They found that there were indeed some males producing new offspring long after they had disappeared from the population.

Because only unmated juveniles were initially included in the introduction, the population started out with zero “dead reproductives” (males producing offspring after disappearing from the population), but the number of dead reproductives gradually increased as time passed. The proportion of dead males that remained reproductively active maxed out at about 25% of the total population. The individual male guppies may have been gone, but their sperm was getting along just fine in their absence.

Out of the 278 male guppies included in the study, just over half had at least one successful reproductive event. Only about half of those that successfully reproduced did so only while they were alive. Another third reproduced both before and after their deaths, and a persevering 15% managed to reproduce only after their demise. So it turns out that being dead is not necessarily a barrier to successful reproduction for these guppies. But why? And what does this tell us about guppy ecology?

Why do it, dad?

Guppy mortality patterns show extreme seasonal spikes for males, with a sharp rise in mortality during the wettest months of the year (July to November). The the females make up for this by acting as living arks for the males’ genes. They essentially act as swimming seed banks: protecting the delicate gametes from challenging conditions and releasing them later, when the environment is more hospitable.

Reznick point out that as long as sperm is stored inside a female guppy’s body, it is essentially “shielded” from selection. This allows the persistence of adaptations that may not necessarily be useful at a given time, but could prove to be valuable for increasing genetic diversity at some point in the future.

This reproductive pattern could have profound benefits for a species that often exists in small, isolated populations. If females are carrying the sperm from previous partners, this can increase both the diversity of gametes available and the effective population size. More genetic diversity will relieve risk the risk of genetic bottlenecks, which frequently plague small, isolated populations. Also, this study lasted less than a year. Female guppies may store sperm for even longer than is reflected by the present data.

Fancy those colours? thefixer

Sperm storage may also allow female guppies to produce sons that are more attractive to other females. Previous research has shown that guppies exhibit a variety of colour polymorphisms, and that females tend to prefer males exhibiting rarer colour patterns. If a mother guppy can mate with a male of a particular colour, there is a chance that by several male generations down the line that colour pattern will be rare or non-existent. When the female guppy finally uses her banked sperm, she will have an exotic looking son that should be highly preferred by other females. Having a popular son is beneficial to both males and females, as it means that their genes are more likely to be carried into future generations.

This also creates an unusual situation: males may face competition both within their own cohort and with older males that may have died before the current crop of suitors had even hatched. There is some evidence for “last-male precedence” (fresher sperm being preferred for fertilisation), which gives an advantage to the young guys, but they cannot entirely escape the fact that their predecessors’ sperm is still on the market.

The implications of this discovery are noteworthy. The study unveils a new mechanism that animals can use to maintain genetic diversity, and shows that male reproductive fitness may not necessarily depend upon long-term survival. The news should also spur researchers to take a second look at other animals that are known to store sperm, such as ants, bees, sharks and even bats.

This an edited version of a post that was first published on Anne-Marie Hodge’s blog.

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