‘Dead’beat Dads: First Evidence of Posthumous Reproduction


All organisms have an evolutionary imperative to maximize the number of offspring they produce. We work within a finite lifespan to successfully pass on as many genes as possible, however: so many gametes, so little time. Some strategy must be involved, right?

Given the inescapable time constraints, many aspects of animal social structure are centered around producing as many healthy offspring as possible during a lifetime. From butterflies surviving only one month to elephants that live for sixty years, every species has a reproductive strategy tailored to make the best use of its allotted time on earth. For example, the antechinus, a tiny marsupial carnivore, has a “live fast and die young” pattern (also known as “big bang reproduction”) in which the males literally mate for two weeks straight. In the process, they bring themselves to such a state of exhaustion that their immune systems fail, and they die. This behavior may seem like a rather unwise choice, but it seems to work for them.

Antechinus. Looks innocent, doesn't he? Don't be fooled.

While most animals don't handle the pressure to propagate quite as dramatically as the antechinus, there is still a universal need to maximize reproduction during a given lifetime. Which brings us to an interesting question: what if an animal could make an arrangement such that more and more of its offspring would be produced for generations after its death?

Well, it appears that the Trinidadian guppy does just that. A recent paper in the Proceedings of the Royal Society B reports that female Trinidadian guppies (Poecilia reticulata) can store sperm and continue to use it to fertilize eggs for generations after a male’s demise (López-Sepulcre et al. 2013).

Male and female Trinidadian guppies

The principal investigator of the study, David Reznick, has been studying Trinidadian guppies for many years. The species can exhibit relatively fast evolutionary responses, making it a great model for answering questions about evolutionary ecology, mating systems, and many other topics. Collecting longitudinal data also creates opportunities for insights about the species’ natural history that might be missed in short-term studies.

Earlier research showed that female guppies have special adaptations for storing and nourishing sperm after they mate (Gardiner 1978; Kobayashi & Iwamatsu 2002), and lab experiments demonstrated that these females can produce young long after they have been removed from the presence of males (Winge 1937). In addition, 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 of these bits of accumulated information led Reznick’s group to a question: given the sperm storage capabilities of females, and the fact that they outlive males by a long shot, is it possible that some sperm is technically fertilizing eggs and producing offspring after the father himself is dead? It sounds like either a fantastic party trick or the plot of a low budget horror movie: definitely worth investigating.

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 population was contained within this locality by two waterfalls book-ending the introduction site. The researchers put the guppies in tanks to mate, then released them into the LaLaja. They returned at regular intervals to capture the guppies and collect both demographic information and DNA samples.

Baby guppy

When it became apparent that there were more fathers producing offspring than there were reproductive males in the population, the team decided to analyze the demographic and genetic data to determine 1) whether posthumous reproduction was occurring, and 2) just how common it might be, relative to “traditional” reproduction (i.e., fertilization with the gametes of two living animals). This was a perfect opportunity for such a study, as the animals were already individually marked and had known pedigrees.

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. Posthumous paternity: check.

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 19.7 ± 6.7 per cent of the total population, and a whopping 31.4 ± 0.09 percent of the reproductive population. The individual male guppies may have been gone, but their sperm was getting along just fine in their absence.

From López-Sepulcre et al. (2013)

Out of the 278 male guppies included in the study, 54.6 ± 2.6 percent had at least one successful reproductive event. Out of those that reproduced, just 50.8 ± 4.9 percent did so only while they were alive. Another 33.6 ± 4.1 percent reproduced both before and after their deaths, and a perseverant 15.6 ± 2.8 percent 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?

From López-Sepulcre et al. (2013)

First of all, guppy mortality patterns show extreme seasonal spikes for males, with a sharp rise in mortality during the wettest months of the year (July-November). Yes, it seems funny that a fish experiences die-offs during the wet season, but that's what happens, apparently. The males may be relatively feeble, but the females make up for it 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.

The authors 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 phenotypes that may not necessarily be adapted to conditions at a given time, but could prove to be adaptive and 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 ("ghost males," if that helps you visualize the scenario), this can increase both the diversity of gametes available and the effective population size. More genetic diversity will relieve risks brought on by the founder effect, which frequently plagues small, isolated populations. It is also noteworthy that this study lasted less than a year. Female guppies may very well store sperm for even longer than is reflected by the present data, something that should be explored in future studies.

Sperm storage may allow female guppies to produce sons that are more attractive to other females. Previous research has shown that guppies exhibit a variety of color polymorphisms, and that females tend to prefer males exhibiting rarer color patterns (Hughes et al. 1999). If a mother guppy can mate with a male of X color, there is a chance that by several male generations down the line, X color pattern will be rare--or, in the case of a founder event, non-existent. When the guppy finally uses her banked sperm, she’ll 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 fertilization), which gives an advantage to the young guys, but they can't entirely escape the fact that their predecessor's sperm is still on the market.

The implications of this discovery are noteworthy: the study unveils a fascinating 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: ants (Holldobler & Wilson, 1990), bees (Baer et al. 2003), sharks (Schmidt et al. 2010; Moura et al. 2011), and even bats (Roy & Krishna 2010). We know that females of those species can save sperm for later use, but the guppy study is the first investigation of posthumous paternity in the wild. Although other animals may not have the same lifespan disparity between males and females that guppies do, sperm storage may still have an "ark" effect if a species goes through a period of high morality rates or seasonal increases in selective pressures. It will be an interesting line of research to follow!

 

ResearchBlogging.org
Baer, B., Schmid-Hempel, P., Høeg, J. T., and Boomsma, J. J. 2003. Sperm length, sperm storage and mating system characteristics in bumblebees. Insectes Sociaux 50: 101-108.

Gardiner, D.M. 1978. Utilization of extracellular glucose by spermatozoa of two viviparous fishes. Comparative Biochemistry and Physiology A. 59: 165-169.

Holldobler, B. and Wilson, E. 1990. The Ants. Belknap Press, Cambridge.

Hosken, D.J. 1997. Sperm competition in bats. Proceedings of the Royal Society B 264: 385-392.

Hughes, K. A., Du, L., Rodd, F. H., and Reznick, D. N. 1999. Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata. Animal Behaviour 58: 907-916.

Kobayashi, H. and Iwamatsu, T. 2002. Fine structure of the storage micropocket of spermatozoa in the ovary of the guppy Poecilia reticulata. Zoological Science 19: 545-555.

López-Sepulcre A, Gordon SP, Paterson IG, Bentzen P, & Reznick DN (2013). Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies. Proceedings of the Royal Society B 280 (1763) PMID: 23740786.

Moura, T., Serra-Pereira, B., Gordo, L.S., and Figueiredo, I. 2011. Sperm storage in males and females of the deepwater shark Portuguese dogfish with notes on oviducal gland microscopic organization. Journal of Zoology 283: 210-219.

Roy, V. K. and Krishna, A. 2010. Evidence of androgen-dependent sperm storage in female reproductive tract of Scotophilus heathi. General and Comparative Endocrinology 165: 120-126.

Schmidt, J., Chien-Chi, C., Sheikh, S., Meekan, M., Norman, B., and Jeoung, S.J. 2010. Paternity analysis in a litter of whale shark embryos. Endangered Species Research 12: 117-124.

Winge, Ö. 1937. Succession of broods in Lebistes. Nature 140, 467.

 

Photo sources:

Antechinus

Baby guppy

Adult guppies


One Response to “‘Dead’beat Dads: First Evidence of Posthumous Reproduction”

  1. Aristarkhos Reply | Permalink

    This is very very interesting. Is this specific to Trinidadian guppies only? There have been times when I have been told by a friend that their guppies have conceived even though they were sure the shopkeeper sold a pair of females. If it isn't endemic to just the Trinidadian then it would be awesome to let them know of about ghost parents. :)

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