Why sex?

05

By Xiang-Yi Li

Department of Evolutionary Biology and Environmental Studies, University of Zurich, Winterthurerstrasse 190, CH-8057 Zurich, Switzerland

What comes to mind when you think about sex? Beauty and love? Or risk and danger? No matter in which direction your emotions lead, one simple fact that we all agree on is rather straightforward – sex is how we makes babies. But why do we need sex to make babies, rather than simply cloning ourselves? In fact, we humans are not special at all in this respect – most species on the planet reproduce sexually. A recent survey found only 22 fish, 23 amphibians and 29 reptiles that can reproduce without sex – a tiny fraction of the more than 42,000 known vertebrate species [1-2].

Sex is expensive. Here I’m not talking about the amount of time, money, or strategic thinking a man may spend in order to win the affection of his dream lover (or the other way round) – those are for social scientists and romantic story writers. The costs of sex that evolutionary biologists are interested in are much more down to Earth.

First, reproducing sexually is extremely inefficient compared to asexual reproduction; in fact, it is only half as efficient. Think about the following scenario: assume that a female is able to produce 2 offspring each year no matter if she reproduces sexually or by cloning. In the former case, the (red) female produces one daughter and one son – meaning that only half of her offspring (the daughter) can directly contribute to population growth; but in the latter case, the (purple) asexual female makes two exact copies of herself, and thus both of them can continue copying themselves to make granddaughters.

409774943080427997-01In addition, sexual reproduction is also very slow compared to cloning. To reproduce sexually, the cell has to go through a complex process called meiosis, which involves the crossover of chromosomes and recombination of genetic materials, and usually takes more than 10 hours [3]. In contrast, cloning reproduction requires a much simpler cellular process called mitosis that only requires straightforward copying of the genome and one single cell division into two identical daughter cells, which can take as little as 15 minutes. The time cost is trivial for species that take a long time to reach maturity and have long intervals between two consecutive reproductive events, like most large multicellular plants and animals, but can be huge to microscopic – especially unicellular – organisms [4].

The most eye-catching costs of sex are manifested through ecological interactions, through sexual selection, mate competition, and sexual conflict. The brilliant long trains (tail feathers) of peacocks are extremely attractive to peahens, but at a cost of increased risk of mortality, as the beautiful colours not only attract mates but also predators, and the weight and size of the long train make it hard to escape. In addition, many species of female spiders and mantis notoriously eat their mates before, during, or after mating. Even more astonishingly, the males of a small shrew-like marsupial called antechinus, literally mate themselves to death [5]. Male antechinus stop making sperm cells before the start of the 2-3 weeks long mating period, during which they frantically search for females and try to mate with as many as possible. They are observed to mate continuously for 6 to 12 hours for several nights in succession and spend little or no time searching for food. As the mating period proceeds, the males lose weight, their fur falls off, their eyes go blind, they bleed internally, and eventually they all die painfully as their immune systems crash completely, a few weeks before their first birthday. It might sound crazy, but such “suicidal breeding” is precisely the solution that natural selection has tailored for the utmost fiery and unforgiving mating competition.

As sexual reproduction needs both males and females, but the two sexes have different needs for reproductive success, sexual conflict often arises and contributes to the cost of sexual reproduction. The best strategy for males often is to mate with as many females as possible, since producing sperm is relatively cheap. As males (especially mammals) seldom help females with parental care, they’re essentially competing against each other in the competition of fathering the finite number of offspring that will be produced by all local females. For females, as producing eggs and taking care of offspring are much more costly, they are more interested in choosing a mate that is either of high genetic quality or provides resources (e.g. defending a foraging territory and/or protecting the females against the harassment by other males). In fact, as mating costs time (which can be otherwise used to search for food or take care of offspring), may attract predators and increase the risk of getting infected with sexually transmitted diseases, females often actively avoid or defend against male mating attempts. In the extreme cases, sexual conflict can cause males to directly harm females physically, or indirectly through infanticide of their offspring, so that the females are forced to stop investing in the offspring of other males and return to sexual receptivity more quickly. Infanticide may sound brutal, but is an effective (if not the only) way for males to gain any paternity in some species. We use lions as an example to illustrate this. Gestation in lions takes nearly 4 months, and mothers do not resume sexual activity until their cubs are about 18 months old. But once a female loses her dependent cubs, she can resume sexual activity within a few days to weeks. In contrast to the minimum 22 months that a female has to spend in order to raise her cubs to independence, the time period that a group of males (coalition) can keep control of the territory of their group is extremely short. For small coalitions with only one or two males, the period is often less than 25 months, and even for large coalitions with 4 to 6 males, the tenure period seldom exceeds 50 months [6]. Therefore, for lions it is a race against time to father any offspring of their own, and only those who managed to force females to return to receptivity quickly (by killing their dependent cubs) may succeed on the battle field of evolution.

Having considered all the (often tremendous) costs of sexual reproduction compared to self-cloning, if you start to feel confused about why sex is still so widespread in nature, then congratulations, you’re now thinking like an evolutionary biologist. Actually, the evolution of sex is such a longstanding puzzle and conceals so many mysteries that it is called “the Queen of problems in evolutionary biology”. Today it is well-accepted that the last common ancestor of all eukaryotic life on Earth had already been reproducing sexually (dating back to roughly one billion years ago [3]), since the same set of genes and basic cellular mechanisms involving meiosis (the most important step in sexual reproduction) is found in all the major eukaryotic branches of the tree of life, including animals, plants, and fungi.

Since sexual reproduction has existed for so long and is so wide-spread through the tree of life despite all the apparent costs, it must also bring even greater benefit. The exact forms of the benefit, however, are still open to debate. The two most influential theories to date are related to either the accumulation of harmful mutations in asexual species or the advantage of sexual species in host-parasite coevolution, with the nick names of “Muller’s ratchet” (named after the Nobel laureate Hermann Joseph Muller) and the “Red Queen hypothesis”, respectively [7]. Both theories are based on one fundamental difference between sexual and asexual species: asexually produced offspring are all identical to each other, while sexually produced ones exhibit far greater diversities in both their traits and genomes.

The “Muller’s ratchet” theory recognises that even though the replication of DNA is generally very accurate, it still carries with it a small chance of making mistakes, in the form of genetic mutations.  These mutations are much more likely to be harmful than beneficial, and in species that reproduce only by cloning, daughters will have genomes that are identical to their mother except a few mistakes, and new mistakes will be added in the next generation when the daughters themselves reproduce, and the cycle goes on and on – unidirectional and irreversible like the movement of a ratchet. After generations and generations, the small mistakes pile up and make the descendants weaker and weaker compared to their ancestors. The accumulation of detrimental mutations can be rescued, however, in sexually reproducing species. Of course, mutations will still happen when making eggs and sperm cells, but these mutations happen randomly and tend to be located in different places of the genome. Therefore, when an egg and sperm merge to create offspring, the reshuffling of genetic materials will create some unfortunate offspring that have lots of bad mutations, while some lucky ones will have none, or even a few beneficial ones. Under natural selection, the offspring with the best genetic quality will have higher chances to survive and reproduce, and the ones with high loads of detrimental mutations will be purged out from the gene pool. In this way, sexually reproducing species can maintain or even improve their genetic quality and therefore outcompete the corresponding asexual ones which suffer from the ratchet-like effect of mutation accumulation and genome deterioration in the long run.

The other most influential theory, the “Red Queen hypothesis”, is named after the Red Queen in the children’s story by Lewis Carroll, Through the Looking-Glass [8]. In the story, while Alice has been running hand-in-hand with the Red Queen as fast as she can until she is out of breath, she finds the trees and the other objects in her surroundings never change their places at all. Surprised and puzzled she told the Red Queen that in her country, if she keeps running very fast for a long time, she will get to somewhere else, but the Red Queen replied, “Now, here (the looking-glass land), you see, it takes all the running you can do, to keep in the same place”. The Red Queen’s race has been used by evolutionary biologists as an analogy to the coevolutionary dynamics between hosts and their parasites.

Imagine a species that reproduces by cloning. Initially the population grows fast and is teeming with individuals that are identical to each other, until a killer parasite (e.g. flu, HIV, malaria, etc.) comes. If the parasite is capable of killing one individual in the population, it can also kill the rest, since all the cloned individuals have exactly the same genetic weaknesses. In this scenario, the parasite spreads like a wildfire until every single member of the host species is wiped out. But in a sexually reproducing species, the same killer parasite normally cannot spread very far. Because all individuals are different, sooner or later the parasite will encounter some individuals that are so different that they are effectively resistant to infection. To spread to the rest of the population, the parasite needs time to mutate its genome and evolve. Over that time, though, the parasite-resistant hosts have already made offspring that are again different from themselves by reshuffling their genomes via sexual reproduction. As a result, some of the offspring are again one step ahead of the killer parasite. Just like it takes all the running for Alice to stay at the same place in the looking-glass land, for the hosts to survive and stay just a little bit ahead of the fast-evolving parasite, they need sexual reproduction to constantly shuffle and recombine their genomes to create diverse offspring.

It is important to note that the two theories are not mutually exclusive, but rather complementary. Despite the fact that the evolution of sex is a long-standing field of research, it is still rapidly advancing, and new theories are continuous being proposed. For example, the author of this article and colleagues proposed a new theory last year, which considers sexual reproduction as a risk-spreading strategy called “bet-hedging” [9]. The new theory considers both the downside of sexual reproduction (producing fewer offspring) and the advantage of it (producing diverse offspring), and use the competition between sexual and asexual reproduction as a metaphor for a lottery scenario. Asexual reproduction is like buying a large number of tickets that all have the same numbers, while sexual reproduction corresponds to buying fewer tickets, but s each having a different number. As the winning number is not predictable, betting on a single number may sometimes lead to a huge win, but most times, it results in a total loss. In contrast, betting on a diverse set of numbers may never lead to a large return, but one also does not lose completely most of the times. Similarly, as the environmental conditions can fluctuate unpredictably (who knows whether the next spring will be warm or cold, rainy or dry?), once the environmental conditions exceed the tolerance range of a clonally reproduced individual, the entire population will die out. The sexually reproducing species, in contrast, produce fewer but more diverse offspring, so that no matter how the environment fluctuates, there are always survivors who will make it to the next generation. The “bet-hedging” (or simply “don’t put all your eggs in one basket”) theory of sexual reproduction provides an additional layer of explanation to the evolution of sexual reproduction.

So far, we have been talking about the costs and benefits of sexual reproduction; now let us jump out of the financing book and think a little more about the process itself. For sexual reproduction to happen, we need a male and a female to come together and… But wait! Why do we need a male and a female? And what exactly are males and females after all? In fact, such “childish” questions are not so straightforward to answer. The definitions of male and female are not about appearances: in some species the two sexes look almost exactly the same, and in others, like the eclectus parrots, males and females display different colours, but both are equally brilliant and colourful. It’s not about size: in mammals the males are often larger, but in fishes, spiders and many insects, females can be much larger than males [10]. It’s also not about dominance and aggressiveness, not about the devotion to parental care, and even not about sex chromosomes: many species simply don’t have them and sex is determined by temperature and other environmental cues during development, such as alligators and turtles. The most important distinction between males and females turns out to be, probably surprisingly, functional – male is the sex that produce small and mobile reproductive cells (sperms) and female is the sex that produce large and nutrition rich reproductive cells (eggs). But even such a general definition only works with species that have only two distinct sexes. (Yes, there are species that have more than 2 sexes. The champion so far is a mushroom Schizophyllum commune, which has more than 23,000 different sexes! [11]) Species that can produce both sperms and egg cells are called hermaphrodites.

The term of hermaphrodite is named after Hermaphroditus, and his/her (slightly tragic) story. In Greek mythology, Hermaphroditus was born as a little boy who grew up happily and became an extraordinarily handsome young man, so far so good, until a water nymph fell in love with him. Since the water nymph was so deeply and fervently in love, she prayed to be united with him forever and never to be separated, and a god (behaving more like a crazy biologist) answered her prayer and literally merged them into one – so from then on, Hermaphroditus (now the forever united couple) has both his male genitalia and a female body. Ridiculous as it might sound, Hermaphroditus’ story does tell us something true about hermaphroditism: if you live a solitary life and only rarely encounter a potential mate (like the water nymph, most probably), once you do find another member of your species, it is better to be able to mate regardless of their sexual traits. No matter whether the other has sperm cells or egg cells, one can ensure reproduction is possible by being a hermaphrodite, and then it’s prepared for both. “Smart for the water nymph,” you might think, but biology adds a tragic twist and turn also for her – hermaphrodites often cannot self-fertilize, so that even though she is united with her love forever, they might never be truly united. Another tragedy is also rather obvious – once you’re a hermaphrodite, you are always in the grey zone and are unlikely to ever appear too attractive to either males or females. Just like a jack of all trades is a master of none, hermaphrodites can specialise in neither male nor female functions, and they can never out compete the sexual specialists (with distinct males and females) except under the condition where mate encounter is rare. Indeed, the hermaphrodites (or simultaneous hermaphrodites to be precise) in nature are often sluggish and solitary invertebrates, such as snails, slugs, and earth worms [12].

If it is too hard to excel at being both a male and a female at the same time, the astute readers might have already asked, why not specialise in one of the sexes and change to the other when needed? Yes, such a strategy has indeed evolved in many species, most commonly in fish, and the direction of sex change is often associated with the mating pool [13]. Under polygyny, individuals usually start as females and then change to males when they are large enough to be able to control a territory and a harem of females; while under monogamy or random mating, individuals usually start as males and change to females subsequently, as both the quantity and quality of eggs are much greater in large females than small ones, but even small males are able to produce enough good sperms for fertilising his mate. Although changing sex is a time and energy consuming process, it can pay off for species where predation risk is very high. For example, in coral-dwelling gobies, if two fish of the same sex find themselves in the same coral head, it’s a much more prudent and evolutionarily successful strategy for one of them to change sex rather than swimming a few meters to another coral head to find individuals of a different sex. For small fish like the gobies, surrounded by many big hungry mouths in the coral ecosystem, even swimming just a few meters can be life-threatening, and thus changing sex becomes a worthy compromise. The author’s favourite species of sex changers, however, is a marine polychaete worm Ophryotrocha puerilis [14]. The worms are monogamous, and within a pair, initially the larger one takes the role of a female while smaller one becomes a male – this makes sense because a larger female can make more eggs while a male does not have to be large to make enough sperm to fertilise them. But as producing eggs cost much more energy than producing sperms, the male grows quicker and eventually becomes larger than the female. Then they both change sex, so that the larger one switches from husband to wife and takes over the demanding job of egg producing, until the other one becomes larger again. The cycle goes on and on between the devoted couple until death do they part.

While the field of research on the evolution of sex has been continuously and actively advancing, evolutionary biologists are still far from a comprehensive understanding of sex and its countless associated aspects. For example, the Amazon molly fish has recently challenged all the major theories of sex evolution [15]. The small fresh water fish reproduces by cloning, but even after 500,000 generations, there is no apparent decay in their genomic quality, and they’re also doing pretty well with the parasites and the changing environment. This new discovery – and many more that are still to come – will continue to fuel the enthusiasm of scientists to challenge the Queen of problems in evolutionary biology. If we’re fortunate, the Queen residing in the diverse tree of life will also continue to reveal to us her endless secret.

References:

  1. Vrijenhoek, R., Dawley, R., Cole, C. & Bogart, J. in Evolution and Cytology of Unisexual Vertebrates (eds Dawley, R. & Bogart, J.) 19–23 (Univ. State New York, New York, 1989).
  2. Wilson, E. O. The Diversity of Life (W. W. Norton, New York, 1992).
  3. Otto, S.P. (2009) The evolutionary enigma of sex. Am. Nat. 174, S1–S14
  4. Lehtonen, Jussi, Michael D. Jennions, and Hanna Kokko. “The many costs of sex.” Trends in ecology & evolution 27.3 (2012): 172-178.
  5. Bradley, A. J., I. R. McDonald, and A. K. Lee. “Stress and mortality in a small marsupial (Antechinus stuartii, Macleay).” General and comparative endocrinology 40.2 (1980): 188-200.
  6. Packer, Craig, and Anne E. Pusey. “Adaptations of female lions to infanticide by incoming males.” The American Naturalist 121.5 (1983): 716-728.
  7. Hartfield, Matthew, and Peter D. Keightley. “Current hypotheses for the evolution of sex and recombination.” Integrative zoology 7.2 (2012): 192-209.

  8. Full text of the book is available on The Project Gutenberg EBook website: https://www.gutenberg.org/files/12/12-h/12-h.htm
  9. Li XY., Lehtonen J., Kokko H. (2017) Sexual Reproduction as Bet-Hedging. In: Apaloo J., Viscolani B. (eds) Advances in Dynamic and Mean Field Games. ISDG 2016. Annals of the International Society of Dynamic Games, vol 15. Birkhäuser, Cham
  10. Fairbairn, Daphne J. Odd couples: extraordinary differences between the sexes in the animal kingdom. Princeton University Press, 2013.
  11. Kothe, Erika. “Tetrapolar fungal mating types: sexes by the thousands.” FEMS microbiology reviews 18.1 (1996): 65-87.
  12. Heath, D. J. “Simultaneous hermaphroditism; cost and benefit.” Journal of Theoretical Biology 64.2 (1977): 363-373.
  13. Munday, Philip L., Tetsuo Kuwamura, and Frederieke J. Kroon. “Bidirectional sex change in marine fishes.” Reproduction and sexuality in marine fishes: patterns and processes (2010): 241-271.
  14. Berglund, Anders. “Sex change by a polychaete: effects of social and reproductive costs.” Ecology 67.4 (1986): 837-845.
  15. Warren, Wesley C., et al. “Clonal polymorphism and high heterozygosity in the celibate genome of the Amazon molly.” Nature ecology & evolution 2.4 (2018): 669.

Additional resources for interested readers:

  1. Miller, Geoffrey. The mating mind: How sexual choice shaped the evolution of human nature. Anchor, 2011.
  2. A database of eukaryotic sex determination systems: http://treeofsex.org/
  3. Schilthuizen, Menno. Nature’s Nether Regions: What the Sex Lives of Bugs, Birds, and Beasts Tell Us about Evolution, Biodiversity, and Ourselves. Penguin, 2015.
  4. Judson, Olivia. Dr. Tatiana’s sex advice to all creation: The definitive guide to the evolutionary biology of sex. Macmillan, 2002.
  5. Bondar, Carin. Wild Sex: The Science Behind Mating in the Animal Kingdom. Pegasus Books, 2016.