ZOOL 304

Sex and Evolution

• Three specific questions are addressed here.
  • Why sex?  Why is sexual reproduction so common?
  • Why do animals often display extreme sexual dimorphism in secondary sexual characteristics?
  • Why the is the sex ratio in animals almost universally 1:1?
     
• Often, these facts are treated simply as basic descriptive observations in biology.
• But each of these problems is, in its own right, a major conceptual challenge for evolutionary biology.

Outside link (Nature Reviews / Genetics, April 2002)

More references:

• Maynard Smith J. (1978) The Evolution of Sex. Cambridge University Press
• Bell G. (1982) The Masterpiece of Nature: the Evolution and Genetics of Sexuality. University of California Press Maynard Smith J. (1978) The Evolution of Sex. : Cambridge University Press
• Vrijenhoek R.C. (1984) Ecological differentiation among clones: the frozen niche variation model. In: Wöhrmann K. and Loeschcke V. (Eds) Population Biology and Evolution. (pp. 217-231). Springer-Verlag
• Hamilton W.D. et al. (1990) Sexual reproduction as an adaptation to resist parasites (a review) Proc. Natl. Acad. Sci. U. S. A., 87:3566-3573.
• Peck J.R. et al. (1998) Explaining the geographic distribution of sexual and asexual populations. Nature, 391:889-892.
• Birdsell J.A. and Wills C. (2003) The evolutionary origin and maintenance of sexual recombination: a review of contemporary models. Evolution. Biol., 33:27-138.

The following notes (and quoted section headings) are adapted from Chapter 6 of Mark Ridley's textbook, EVOLUTION, 2nd ed. (1996), Blackwell Science, Inc., Cambridge MA. ISBN 0-86542-495-0.

"Sex is the queen of problems in evolutionary biology."  (Graham Bell, 1982)

• "Sex has a 50% cost."

  • This is the fundamental difficulty.  Whatever advantage (if any) sex has, it must be sufficient to outweigh this huge cost, if sex is to be properly considered as an adaptation.
  • Even in hermaphroditic species, the cost is maintained by selection for balanced investment in male and female gamete production (see sex ratio, below)
  • Several hypotheses have proposed to explain what adaptive advantage might override this cost.
     
• "Sex can accelerate the rate of evolution."
  • Sex makes possible the recombination of alleles at various loci.  Bringing together favorable alleles, rather than waiting for coincidence mutation, can accelerate the pace of adaptation.  This does seem to be a definite and undisputed advantage for sex.
  • Unfortunately, sex can also break up favorable combinations of alleles.  So, this does not like a clear and universal benefit sufficient to outweigh the 50% cost of sex.
     
• "Is sex maintained by group selection?"
  • The acceleration of evolution should be favored by group (i.e., species) selection, based on both a higher rate of speciation and lower rate of extinction.  These processes are the species-level analogues of reproduction and survival for individual selection.
• One difficulty with this explanation is that individual selection is expected to be much faster and more effective than group selection.  Individual selection, therefore, should consistently override group selection whenever the two levels operate at cross purposes.
• Some species (notably aphids) strike a "balance" between sexual and asexual reproduction.
  • Since both strategies are clearly available for individual selection, this is taken to imply that both strategies are advantageous for individuals.  (Otherwise, one or the other strategy would be eliminated by selection.)
  • Therefore, in aphids sexual reproduction must have a strong enough advantage for individuals to balance asexual reproduction.
  • If that individual advantage exists for aphids, a group selection explanation may not be needed elsewhere.
  • We still do not know what that individual advantage really is.
• Arguments based on group selection cannot (yet) explain the function of sex (i.e., thay cannot explain how selection for accelerated evolution can override selection for efficient reproduction.)
• But we still don't have a good individual-selection explanation, either.
   
• "Sexual reproduction can enable females to reduce the number of deleterious mutations in their offspring."
  • This proposed function for sex is a complement to the one above.  Just as sex can bring together "beneficial" new mutations, it can keep together a set of established, successful alleles.
  • Otherwise, in asexual lineages, deleterious mutations could and would accumulate in spite of selection.
    • Occasionally, every offspring will carry at least one deleterious allele.
    • Under such circumstances, the best that selection can do is find the least disadvantaged genotype.
    • From that point on, the least-deleterious allele will be fixed.
    • As this process repeats, deleterious alleles will accumulate, until viability is compromised for the entire population.
    • This is sometimes called "Muller's ratchet" or "mutational meltdown".
  • This hypothesis can be developed quantitatively.  At a high enough rate for deleterious mutations, sex can provide sufficient advantage to outweigh the 50% cost.  However, it is seems to require unrealistically high mutation rates (although mutation rates are notoriously difficult to measure).
  • Certain organisms (e.g., some rotifers) seem to have escaped Muller's rachet.  Molecular evidence indicates that bdelloid rotifers have been asexual but have been so for a long, long time.  (more)  (more)
     
• "The coevolution of parasites and hosts may produce rapid environmental change."
  • If environments change fast enough, successful reproduction from one generation to the next may demand that offspring NOT resemble their parents too closely.  Leigh Van Valen introduced the Red Queen hypothesis to describe this situation.
  • Under such circumstances, sex may be advantageous.
  • The difficulty is finding a change which is BOTH sufficiently extreme to override the 50% cost AND common enough to explain the near universality of sex.
  • Rapidly evolving parasites are proposed as a selection pressure upon the hosts which changes rapidly enough to fit the bill.  And parasitism (by viruses, bacteria, protists, etc.) is practically universal.
  • Detailed knowledge of the genetics of host-parasite interactions is still inadequate to confirm or refute this hypothesis.
     
• "Conclusion:  It is uncertain how sex is adaptive."
  • Where do these hypotheses stand?
  • Description (testing by consistency with expectations) has not demonstrated an adaptive benefit sufficient to outweigh the cost.
  • Experimentation is not practical.  We lack the ability to manipulate sexuality as a reproductive strategy.
  • The comparative approach, which is necessarily indirect and circumstantial, proves that sex must be advantageous (it is maintained under nearly circumstances, while its loss appears to be a "terminal" adaptation").  Special cases like aphids provide suggestive evidence that an advantage to individuals exists, but do not reveal what that advantage is.
  • There remains a gnawing suspicion that, in the words of John Maynard Smith, "some crucial aspect of the problem has been overlooked."
    • Your professor suspects that what has been overlooked is the possibility of something like group selection (see Chapter 10) successfully suppressing the potential for asexual reproduction to evolve.
    • By this hypothesis, asexual reproduction would indeed evolve to take advantage of the 50% cost of sex, if only asexual variants appeared.  But sex has become is so enmeshed in other features of genetic architecture that asexual the variants arise too infrequently for asexual reproduction to prevail.  
    • In species in which this genetic constraint has been reduced, individual selection for short-term individual advantage can indeed lead to loss of sex.  But then the species itself loses facility at adaptation and becomes more vulnerable to extinction.
    • An analogy can be drawn with cancer.  Here, selection based on immediate advantage for individual cells can indeed be very rapid and can overide advantage to the organism.  But organisms have evolved mechanisms to suppress the appearance of independently evolving cells.  Short term advantage (cancer growth) can indeed win out, but only if it's allowed to get started.  By analogy, then, asexuality may also be a winning strategy (as implied by the 50% cost of sex) in the short term but terminal (leading to extinction) in the longer term (as implied by the limited phylogenetic distribution of asexual species); therefore, those lineages which persist are those which successfully suppress the origination of asexual variants.

Why are two sexes so different?  The effects of sexual selection (i.e., selection based on competition for access to complementary partners for sexual reproduction).

• "Sexual characters are often apparently deleterious."
  • We must, therefore, ask how such characters can evolve (i.e., ordinary natural selection against some deleterious effect of the character can be overcome).
  • Sexual characters which are NOT deleterious pose no explanatory difficulty; these will not be discussed here even though there is a rich literature.
  • Note how both experiment and comparative study have been used to support the following hypotheses.

• "Sexual selection acts by male competition and female choice."
  • Comparative study, beginning with Darwin, provides extensive evidence that sexual dimorphism is more pronounced in species where individuals compete more strongly for mates, and that the sex (usually male) which competes has the more extreme character development.

• "Females may choose to pair with particular males."
  • When females are passive, and males simply fight with one another for access, explanation of adaptation by sexual selection is straightforward and relatively unproblematic.
  • However, when females actively choose, and males compete to be chosen, it becomes somewhat more difficult to understand why females would choose males with deleterious traits.
    • Once the mating pattern is established, then females become obliged to choose the "preferred" type of male, or their male offspring will be less successful at finding mates.  So, it is fairly easy to understand how female choice even for otherwise deleterious traits can be maintained in a population after it has become established.
• The problem is understanding how selection could establish such a mating pattern in the first place.  Several models (hypotheses) have been proposed for how this could work.
   
• Fisher's "runaway sexual selection" model.
  • An early form of the trait in question (ancestrally, prior to the effect of sexual selection) would actually be advantageous if exaggerated.
  • Female choice evolves to prefer this the more advantageous, exaggerated trait, because offspring of such females are more fit.
  • Once such female choice has become instinctive, males then face selection pressure from that choice, to exaggerate the trait.
  • The resulting instinctive preference for "larger" will not automatically stop once "large enough" has been reached.
  • The result is runaway sexual selection, in which pressure of female choice drives male trait development beyond the value which would give optimal population fitness.
  • Equilibrium will be reached when the cost of the excessive trait balances the female preference.  At this stage, the trait no longer has any intrinsic fitness value for the population.
     
• Zahavi's "handicap" model.  
  • Females may prefer handicapped males, because their survival indicates indicates high genetic quality.
  • If a male can function in spite of some extravagant handicap, other genes for fitness must be in pretty good shape.
  • The "handicap" then serves as a signal for overall fitness.  

    Human display can serve an analogous role, signalling economic fitness.  Men with low incomes cannot buy fancy clothes and sports cars.  So women who marry flashy men may have some increased expectation of economic resources for child support.

  • Females who prefer males with the "handicap" will assure that all of their offspring get good genes (except, of course, those for the handicap itself).
  • In this model, the selected trait is costly, for both sexes, from the beginning.  But females benefit in other ways from using the costly trait as a signal.
     
• "Female choice in Fisher's and Zahavi's models must be open-ended, and this condition can be tested."
  • In Fisher's model, "runaway selection" depends on positive feedback, in which females consistently prefer a more extreme form of the selected trait (rather than some particular optimal value).
  • In Zahavi's model, females must prefer a larger over a smaller handicap in order to maintain the handicap against selection to reduce it.
  • In fact, experimental manipulation has repeatedly demonstrated that females may prefer trait forms far more extreme that those presented by actual males.  (This is unsurprising, given that evolved instincts simply need to work; they need not be intelligently farsighted).
  • Such experiments show that either Fisher's or Zahavi's model could be true, but do not distinguish between the two models.
     
• "Conclusion: the theory of sex differences is well worked out but incompletely tested."

Why is the sex ratio almost universally 50:50 ?

• "Natural selection usually favors a 50:50 sex ratio."
  • Under most circumstances, a 50:50 sex ratio (males : females) should be an equilibrium value.
  • That is, any departure from this ratio should create conditions (negative feedback) which will restore the equilibrium.
  • A lower proportion of either sex will make that sex disproportionately responsible for the next generation, so selection should favor greater production of that sex, as long as competition for mates is distributed among a large population.  (A similar argument supports the expectation of equal investment in male and female gamete production in hermaphroditic species.)
     

  This circumstance offers some indirect evidence that "group selection" must not be especially effective.  Group selection would be expected to favor a much reduced proportion of males, since the advantage of sex (whatever it is) could be retained while increasing the efficiency of reproduction.  

• "Local mate competition causes deviation from a 50:50 sex ratio."
  • The 50:50 ratio is at equilibrium only if there is a population-wide competition for mates.
  • Under special circumstances, such as in some parasitic wasps where mate competition is not population wide but brothers compete primarily with one another to mate with their own sisters, selection will favor a reduced proportion of males.  The optimal proportion of males will depend on the probability that brothers will compete only with another or with one or more additional sets of siblings.
  • Observed ratios correspond well with theoretical predictions.
     

• "Trivers and Willard identified another case in which sex ratio should deviate from 50:50."
  • In red deer, data suggest that sons of dominant females have higher fitness than daughters, because they outcompete other males for access to many females.
  • Under such circumstances, it should be advantageous for dominant females to produce a higher proportion of sons than daughters, and data confirm this expectation.

Comments and questions: dgking@siu.edu
Department of Zoology e-mail: zoology@zoology.siu.edu
Comments and questions related to web server: webmaster@science.siu.edu