Sex and Evolution

Lecture 06

Email me

Assignments Page

Back to:

• Sexual and Asexual Systems
  • Animals
  • Plants
  • Fungi
  • Bacteria
  • Why not be a simultaneous hermaphrodite?  The Theory of Sex Allocation
• Sex Implications and Costs
• Sexuality and Diploidy
• Sexuality leads to Recombination
• Short-term (ecological?) Costs
• Long Term Costs
• Sex and Developmental Constraints
• Endosymbiont Model
• Potential Benefits of Sex
  • Faster rate of adaptive evolution under Directional Selection
  • Group Benefits
  • Sibling Competition
  • DNA Repair
  • Reduction of Mutation Load
  • Adaptation to Fluctuating Environments (Lottery Model)
  • Pathogen Model
• Sexual Selection
  • Sexual selection is contrasted with natural selection
  • Male Competition for Mates
  • Female Choice
    • Sensory Bias
    • Fisher's Runaway Selection Hypothesis
    • Zahavi's Handicap Hypothesis
  • Intersexual Conflict and Antagonistic Coevolution
• Sex Ratio
• Sex Ratio and Sex Determination
• Fisher's Theory of Sex Ratios
• Does Fisher's theory always apply?
• Under some circumstances, Fisher's theory will not apply
  • Endosymbiosis
  • Group Selection in Metapopulations
  • Related groups and Individual Selection
  • Care for Offspring and Sex Ratio
• Is it really the sex ratio at birth that is most important?

Sexual and Asexual Systems

There is more to this area than just comparing sexuals with asexuals

We should consider some assumptions we make due to our point of view as complex animals

• We contrasted gene versus individual selection in discussing the units of selection but what is an individual?
  • endosymbiosis is common (are we all, to some extent, lichens?)
  • colonial animals, ramets vs. genets in plants, lineages vs cells in yeast and bacteria, all pose problems for defining individuals
• most animals have a distinction between germ-line cells and somatic cells but some colonial animals, plants and fungi do not make such a distinction
  • here, many (sometimes any) portions of the mitotically produced organism (however complex) will undergo meiosis and, as genetic differences can accumulate during many generations of mitosis, gamete genotypes will vary more than in species that separate the soma from the germinal tissue

Animals

• sexuality is fairly uniform in that males produce sperm and females eggs
  • Hermaphroditism means that sexes may not be separate
    • some are simultaneous hermaphrodites (both sexes at once) but some animals are sequential hermaphrodites
      • Protandry - males when small and females when larger (larger females make more eggs but smaller males are as successful as large males)
      • Protogyny - females first and males when larger (species where males must compete for females and size is important in the competition)
  • Most sexual animals are Dimorphic (male and female phenotypes differ in areas other than reproductive systems and genitalia)
• Sexual and asexual reproduction part of a single species' life history
  • some invertebrates have only seasonal sexuality in that they reproduce asexually until some environmental clue (often linked to the changing seasons in temperate regions) triggers the production of males and a single round of sexual reproduction
    • amphidiploids often only produce males after several generations of parthenogenic reproduction
    • sexual reproduction can produce new phenotypes such as
      • resting stage that will overwinter to produce the next year's asexuals
      • dispersal morph that can find overwintering refugia
• Asexual species are often referred to as Unisexual species as the male phenotype is lost
• Ploidy is often a part of asexuality
  • Triploids and tetraploids often have difficulty at synapsis, favoring parthenogenesis
• Asexuality can be attained through:
  • vegetative reproduction - offspring are mitotically produced buds (e. g., Cnidaria)
  • parthenogenesis - females produce diploid eggs that don't need fertilization
• Apomixis - asexuality without any meiosis
• Automixis - meiosis occurs but the gametes that fuse (usually as nuclei from the same meiosis) are from the same parent so that crossing over can occur but no mixing of genes not present in the parent cell
  • this process often leads to increased homozygosity when gametes combine that both have the same allele at heterozygous loci, which eliminated the other allele at that locus in that lineage
• meiosis is sometimes part of asexual life history
  • Gynogenesis - known from some fish and amphibians
    • all-female species produce eggs that are activated, but not fertilized, by sperm from a related species
    • eggs are diploid either because they do not undergo meiosis or because, after meiosis, diploidy is restored by suppression of cell division or by fusion of the egg nucleus with a polar body nucleus
    • diploidy (or more) may be the result of the cells containing haploid genomes from two or three (could be four, but I don't know of any) different, sexual species
    • one of the ancestral species donates the sperm
    • this is sometimes referred to as sperm parasitism because of the necessity for a contribution from a related species
  • Androgenesis - rare but known in some insects
    • after fertilization, male chromosomes are retained and female chromosomes are lost and diploidy is subsequently restored
  • Hybridogenesis - similar to gynogenesis except that eggs are fertilized and the resulting organism is diploid but, at gametogenesis, only female chromosomes get into the gametes
    • only eggs are produced and sperm from a related species is needed (notice that the genes from the sperm are part of the phenotype!  makes for some complex genetic interactions)

Plants

• Plants produce both sperm and pollen
• alternation of generation
• Flowers complicate plant sexuality
• Plants can be bisexual or unisexual, flowers can be the same (perfect or imperfect flowers)
  • Dioecious plants have male and female plants (all flowers have one sex only (= imperfect) and all flowers on a single plant are the same sex, so that the entire plant either produces eggs or pollen
    • Individual plants are either Gynoecious (female flowers only) or Androecious (male flowers only).
    • Asexual plants are often gynoecious but the ova are diploid
  • Hermaphroditic (= Monoclinous) plants have only perfect flowers
  • Monoecious plants have imperfect flowers (separate male and female flowers) on the same plant
    • can be simultaneously (= synchronously) monoecious or sequentially (= consecutively) monoecious
    • sequentially monecious plants may be protogynous (= proterogynous, both are like progynous in animals but botanists used a different latin dictionary) or protoandrous (= protandrous in animals)
      • individual flowers can also be protandrous and produce pollen first or progynous and produce ovules first
    • Subdioecious plants are dioecous species that produce occasional monecious plants
    • Gynomonoecious plants have both hermaphrodite and female flowers.
    • Andromonoecious plants have both hermaphrodite and male flowers.
    • Trimonoecious plants have male, female, and hermaphrodite flowers all on the same plant.
  • Diclinous plants have imperfect (= unisexual) flowers, so the term includes both monoecious and dioecious species.
• The previous terms apply to individual flowers and plants and a separate set of terms are applied to strategies at the population or specific level.
• Hermaphrodite, Monoecious, Gynoecious, and Dioecious populations or species contain only plants with the applicable sexuality
• Polygamous populations and species have both hermaphrodite and unisexual plants
  • Gynodioecious populations or species have both gynoecious (female) and hermaphrodite plants
  • Androdioecious populations or species have both androecious (male) and hermaphrodite plants
• Subdioecious populations are composed of unisexual (dioecious) plants, with some monoecious individuals also.
• Trioecious applies where male, female, and hermaphrodite plants are equally mixed with in the same population.
• The distribution of species is not equal.   About 3/4^ths of all Angiosperms are hermaphrodites.  Of the final 1/4^th, 2/5^ths are either strictly dioecious or monoecious species, another 2/5^ths have both perfect and imperfect flowers, and the final fifth are gynodioecous or androdioecious.

Fungi

• wide range of sexuality
• yeast
  • can be automictic or apomictic
  • because each cell is also an organism, they may undergo many mitotic reproductions between each meiotic event
  • asexual lineages common
  • antiquity of asexual lineages is controversial
  • asexual lineages often show genetic markers of rare sexual events
  • sexuality can be restored to asexual lineages (less complex phenotypes than animals)
• multicellular fungi
  • many have complex life histories (these are often plant parasitic fungi) with one or more asexual stage and a single sexual stage
  • often grow as haploids post spore germination
  • at some time, two haploids fuse to produce mycelium with nuclei from both parents (Plasmogamy)
  • when sexual reproduction is to occur, nuclei fuse (Karyogamy)
  • this life history decouples sex and reproduction (see later under cost of sex section)

Bacteria

• no true diploids formed through fusion of gametes
• genes transferred as segments of DNA absorbed by a cell (transformation) or from viruses containing host rather than virus DNA (transduction), mobile genetic elements, or plasmid exchange (conjugation)

Why not be a simultaneous hermaphrodite?  The Theory of Sex Allocation

• Classic book on the subject (good place to start, lots done in this area since) is The Theory of Sex Allocation by Eric Charnov, 1982, Princeton University Press, Princeton, NJ
  • Lots in book on sex ratio but we will consider only part of the problem of hermaphroditism here
• Assumes that there is a linear tradeoff in energy available for each sexual function
• whether or not a species should be hermaphroditic or dioecious depends on the change in reproductive success of males versus females as resource allocation changes
  • a linear relationship favors neither strategy (hermaphroditism or dioecy)
  • if there is a benefit for being both sexes, then hermaphroditism is favored and the allocation of resource to each sex will depend on circumstance (could range to almost all male to almost all female)
    • Hermaphroditism may guarantee mating success for rare species that experience a real risk that they will not find a mate
    • Sessile organisms, like barnacles, entoprocts, attached tunicates, etc., are hermaphroditic more often than motile organisms (don't know why but may be due to mating risks)
    • Species with a brood pouch (like many anemones, bivalve molluscs, and echinoderms, might use excess energy to make sperm once they had filled their brood pouches with eggs (the proportion of brooding species that are hermaphroditic is higher than the overall proportion of hermaphroditic animal species)
    • plants spend energy on flowers whether they are perfect or imperfect flowers, so the cost of perfect flowers is shared by both sex and less for each sex for that reason
  • if there are extra costs to being both male and female, then dioecy is favored
    • if both male and female functions require separate structures, then a hermaphrodite incurs both costs, while a unisexual individual incurs only one cost and more of the reproductive resources can go directly into offspring

Sex Implications, Costs and Benefits

Sexuality and Diploidy

• consider diploidy, with its costs and benefits, separately from sexuality
• The essence of sex is the production of new combinations of alleles at variable loci
  • sex in diploids produces potentially genome-wide recombination with each sexual event
  • haploid organisms, most importantly bacteria, can still produce offspring that vary but they typically do  so through exchange or acquisition of only a portion of their genome
• although the mechanisms differ, both haploid and diploid sex are legitimately considered sexual recombination
  • however, the costs of sex differ for haploids
  • they do not bear the 50% "growth" cost (see below) but may bear some cost due to longer fission times
  • gene acquisition may entail a material and energetic cost if the new genes replicate independently of the nuclear genome

Sexuality leads to Recombination

• recombination promotes the generation of variation in the sense of increasing the number of combinations of alleles at different loci
• recombination has two levels connected to sex
  • segregation - the reshuffling of chromosome combinations during meiosis
    • each gamete is a random mix of chromosomes from the individual's parents
  • crossover - reshuffles linked genes through reciprocal exchange of DNA between homologous chromosomes (we won't discuss non-reciprocal exchange here)
• haplotypes are broken up with a probability dependent on the distance between loci
• does Recombination carry a cost?   see below under long-term costs for sex

Short-term (ecological?) Costs

• sexuality reduces the maximum potential population growth rate
  • the number of females determines maximum number of individuals in the next generation, so a female that produces males will have fewer grandchildren than if she produced all females
    • this cost assumes that the sex ratio is 1:1 (see later for justification of this assumption) and that sexual and asexual females are equally fit
    • this is called the "two-fold" cost of sex, but it is only true in species where the female gets no help from the male in rearing the young (this reduces the cost proportionately)
  • even where there is an overproduction of offspring, such that not all will live and reproduce, the "growth" cost of sexuality may still be 50%
  • hermaphroditism is not an answer to this cost
    • every individual is a female but an organism's total energy available for reproduction must be split between the sexes, so the cost is measured in gametes, not in individuals
      • hermaphrodites produce fewer eggs than non-hermaphrodites (this has been tested with plants), so there is still a cost to producing sperm or pollen
• Additional Potential Costs
  • Sexuality leads to reproductive failures not found in asexual individuals
    • Failure to find a mate
      • can be critical after bottleneck or after founding of a new population for species not normally rare
    • Post-zygotic incompatibilities due to recombination can cause reproductive failure
    • Egg wastage can occur if females mate with males having incompatible sperm or pollen (different variety, different species)

Long Term Costs

• recombination costs
  • many have wondered why an organism would want to mix its genes with another's
    • favorable combinations of genes will only persist through generations through linkage disequilibrium
    • selection in asexuals should make good gene combinations common but, in sexuals, good combinations are always being broken up by recombination
    • some organisms suppress recombination at the cross-over level (Drosophila males have no crossing-over), suggesting that less mixing is good for at least some species
  • at heterotic loci, the heterozygote individuals will not be able to avoid producing offspring that are less fit while asexuals will preserve the heterozygosity of their offspring as they do not recombine each generation
  • does Recombination provide a benefit?
    • fit genes next to unfit mutations are not linked to those mutations forever

Sex and Developmental Constraints

• below, we examine the question of the costs of sex and why sexual reproduction is common in the face of these costs
  • sex that is uncoupled with reproduction carries fewer potential costs, specifically it bears no "growth" cost
    • in fungi with a dikaryonic life history stage, there is no evidence that the number of potential offspring is decreased by the presence of sex
    • some ciliates exchange nuclei but do not reproduce as a direct part of the process (although mitosis sometime follows the sexual process)
  • if sex arose when it carried little or no cost, it might have persisted as an atavism that we are stuck with, like the use of only L amino acids or the genetic code (or ties for men's formal dress)
    • this would require that it be difficult for sexual species to become asexual
      • the distribution of asexual species argues against this as they are mostly found as "tip species" on an evolutionary tree, indicating that they have recently arisen through loss of sex by an asexual species
      • asexuality has arisen in laboratory populations of Drosophila
  • the process seems less likely to go the other way
    • if asexuals have little of the genetic information needed for meiosis or for the production of male phenotypes, switching to sexuality means acquiring a large amount of information over a short period
• so we may see sex as the primitive condition for eukaryotes and asexuality as the derived condition
  • some single-celled eukaryotes (yeast) may be exceptions as changing one gene may cause sex to be lost and a back mutation may restore sex, so switching may be more common
  • when hybrids form (especially in plants), they may begin as asexuals and regain their ancestor's sexuality, although this seems to be a very rare phenomenon if it occurs (although rare phenomena may be important and we will return to this when we discuss genome duplication)
• so there seems to be no developmental constraint in sexual species becoming asexual and restraint against asexual species becoming sexual

Endosymbiont Model

• Some mitochondria exhibit independent motility by hijacking the host cell's actin filament network
  • they can move in and out of the nucleus and between adjacent cells and might carry genetic material from cell to cell
  • In some cells, mitochondria form clusters and can move the entire cell
• The endosymbiont model (C. Bazinet.   2004.   "Endosymbiotic origins of sex."  BioEssays, 26:558–566.) postulates that sex is the outcome of early prokaryote symbionts causing infected cells to act like sperm
  • This model sees sex originating as a by-product of symbiote behavior which avoids the need to overcome the costs
• there is little actual evidence for this idea, but it does cause one to widen the field and consider that early eukaryote evolution might have been very different from today

Potential Benefits of Sex

Faster rate of adaptive evolution under Directional Selection

• when two beneficial mutations arise in an asexual lineage, the only way to get an organism with the both is to have both occur within the lineage, one after the other
  • the only way to increase the chance of his happening is to wait until the first mutation becomes common through selection and drift
• sexual gene pools can produce organisms with both beneficial mutations more quickly
  • caveat - if the rate of occurrence of beneficial mutations is so slow that one is likely to be fixed in a gene sweep before the next arises, there is no difference between sexual and asexual evolutionary rates
• this effect will also occur when the population size is small (greater fixation rates)

Group Benefits

• I have this heading in our notes only because the book has a discussion of sex favored by group benefits
• the major problem for this is that the group benefits are not specified and as discussed are also benefits that accrue to individuals
  • this means that, if it operates, its effect would not be antagonistic to individual selection but an enhancement and difficult to measure
• we will leave the group benefits discussion here

Sibling Competition

• siblings often live in close proximity and may be the most likely conspecific competing pairs of organisms
• some have reasoned that variation among siblings may allow them to lessen competition to some degree due to differences in requirements, etc. that arise through recombination
• detractors have criticized this model because it may apply only in a small proportion of sexual species

DNA Repair

• In order to repair damaged DNA, an undamaged copy must be at hand but, at polymorphic loci, an undamaged copy can only be obtained through sexual recombination
• this is a universal advantage but has little empirical evidence to support it at this time

Reduction of Mutation Load

• mutations at different loci will often be deleterious and, as they build up in a lineage, they constitute a mutational load
  • as mutations occur, the number of individuals without any deleterious mutations at any loci will dwindle and eventually be lost through drift and selection
• this means the fittest possible genotypes are lost to the population
• then the class of individuals with one deleterious mutations undergoes the same fate
• the next fittest individuals are also lost
• This process is known as Muller's Ratchet and, in asexual lineages, will cause a steady decrease of fitness (assuming all mutations are deleterious)

• in recombining populations, mutations will be combined in the same individuals more often than in asexual populations

  • those individuals with multiple mutations will be less likely to survive and reproduce and this process will eliminate the mutation from the population more efficiently than in asexual populations

    • this is especially true if there are epistatic interactions between mutated loci such that the fitness of individuals with dual (or triple, or more) mutations is less than the product of the fitness loss due to each mutation

      • where + is the non-mutant allele and m is the mutant, for two loci with mutants where
      • survival of ++ haplotypes is 1.0, survival of +m haplotypes is 0.9 and survival of m+ haplotypes is 0.8
      • if the survival of mm haplotypes is less than 0,72 (= 0,9 x 0,8), epistatis is occurring

Adaptation to Fluctuating Environments (Lottery Model)

• This model is an analogy to the best way maximize your winnings in a lottery
  • say tickets are $1 and you have $100 dollars to spend on the lottery.
    • Situation 1 - you know what the winning number will be
    • Situation 2 - you have no idea what the winning number will be
  • What do you do?
    • Situation 1 - buy 100 winning tickets (not just one - remember others may have the winning ticket too and you will get a reward proportional to the number of winning tickets bought)
    • Situation 2 - buy 100 different tickets and pick randomly (it will do as well as any other number-selecting scheme)
• we can reframe this situation for our purposes by making a comparison between knowledge of the winning ticket and knowledge of the winning genotype:
  • when the environment is predictable and the same as the parent's (unvarying environments) the parents genotype is successful enough to survive and reproduce now and, because of the lack of change, will be successful in the future
  • in this situation, asexual reproduction should be favored as it is the winning ticket
  • if the environment is variable, then a parent should "spread its risk" by increasing the variation among its offspring through sexual recombination so that at least some might hold the winning ticket
  • there are two cogent criticisms of this argument
    • environments do not change much between generations, which should favor asexual reproduction, which is contrary to what we see in nature
    • when sexual and asexual populations exist within a species, the asexual is often found in the more variable environment, contrary to the model's expectation
      • some fish that live in freshwater ponds fish vary in their sexuality and the asexuals are more likely to be found in the temporary pools and the sexual populations in the permanent water bodies
      • the difference is probably due to the greater growth rate of asexual populations, which can exploit temporary resources more efficiently than sexual populations

Pathogen Model

• Hamilton (reviewed in W. D. Hamilton, R. Axelrod, and R. Tanese.  1990.  "Sexual reproduction as an adaptation to resist parasites (a review)." Proceedings of the National Academy of Sciences of the United States of America 87:3566-3573.) proposed that it was not variation in the habitat that made genetic variation among offspring valuable but variation in the array of parasites that attack any species
  • this is a variation of the lottery model but the winner depends on being resistant to common parasites found in the population
• by recombining each generation, it is more likely that some of offspring will have resistance to the pathogens present
  • if you are asexual and resistant you are a winner but only if the pathogens do not adapt and become able to overcome resistance
  • if this happens, then a winner today will be a loser tomorrow
  • resistance and virulence genes vary in their frequency in a frequency-dependent manner so they are always changing
• by recombining, offspring are variable and have a better chance of tracking changes in the parasite population
  • this is a case of antagonistic coevolution and a second instance of this phenomenon, involving male versus female conflict, is discussed below

Sexual Selection

For sexual species, populations are now divided into two sexes.  This division has consequences for evolution of the population.  The consequences are usually lumped together under the general heading of sexual selection, but we will start at a deeper level (briefly)

• First, we should discuss a fundamental difference between the sexes, one that leads to many other differences: Anisogamy (or Heterogamy), the production of gametes of different sizes
• Isogamy (or Homogamy) is found only for single-celled and structurally simple eukaryotes, most multicellular species are anisogametic.  Why so?
  • The theory (Brian Charlesworth.  1978.  "The population genetics of anisogamy."  Journal of Theoretical Biology, 73:347-357) is based on the larger size of one gamete being helpful for the survival of the zygote.
  • The small size of the other gamete promotes motility and allows production of sufficient numbers to guarantee fertilization of the large, immobile gamete.
  • Models with individuals that produce these two sizes of gamete and a third type of individual that produces isogametes select for the size extremes at the cost of the intermediate size gamete because the middle size gets no particular benefit and is lost from the population
• Anisogamy leads to a basic difference in reproductive strategies between males and females since the number of eggs produced per female is less than the number of sperm produced per male
• males can mate with many females and choice of a suboptimal female has only small fitness consequences if many matings are obtained
  • females mate with males but one male can supply enough sperm to sire all of her offspring and mating with a suboptimal male has major fitness consequences for her offspring
• There is a second difference that is a natural outcome of anisogamy:variation among the mating success of males is much greater than among females
  • once a female has mated she need not mate again but males can still mate even after mating previously
  • female choose from among a wide range of potential mates but males compete for a limited number of mates
  • in a population of 10 females and 10 males, five matings have taken place and, at this point, the males compete for the remaining five females but the five remaining, unmated females still have ten males among which to choose
  • in fact, only one male may be successful in mating in this population (assuming a male can mate 10 times) and it will produce all the offspring it has the potential to produce

Sexual selection is contrasted with natural selection

• Sexual selection is selection based on differences in reproductive success among members of a single sex
  • sexual selection is responsible for many (not all - some are tied to different ecological roles for the sexes) of the differences between males and females in dimorphic species, especially those related to showy ornaments used for courting during mating
    • one of the dimorphic pair is usually cryptically colored, so it appears there is value in not being apparent to predators and it is likely that the showy member of the pair bears the cost of extra predation as well as any cost involved in the showy structures and colors themselves
    • dimorphism will happen only when there are differences between males and females in the number of matings
      • monogamous species, in which males and females have the same number of matings (one) tend to be monomorphic (think of swans or vultures)
      • polygamous species (polygyny is far more common than polyandry) means that one sex (usually males) may have more matings than the other sex (think of peacocks vs peahens, or ducks, or cardinals)
  • Like group selection vs individual selection, the natural and sexual selection become apparent when they pull in opposite directions
    • The most popular example of this is the male peacock's tail
      • The tail is helpful when the male is mating as peahens choose peacocks based on their ability to display a spectacular tail
      • The tail is not helpful when flying or running and so this character is seen as a result of sexual selection overcoming natural selection

  Sexual selection is the result of two phenomena: male competition for mates and female choice of mates.  So, why do males compete and why do females choose?

Male Competition for Mates

• Males compete for mates because they produce excess gametes and can mate with many females
  • competition can be reversed when males provide the limiting resource
  • in some bird species males rear the offspring and can only care for one clutch of eggs each breeding season and so they mate with only one female each season.  females can produce more than one clutch, so females mate with more than one male each season
  • in these species, the females compete for males and males choose or reject females
• Males can compete by:
  • fighting (think of all of those Nature episodes with male sheep butting heads, deer trying to gouge rivals with their antlers, or huge walruses gashing each other with those huge tusks
    • often males have ritualized fights that produce a winner in terms of breeding but no loser in terms of injury, so the loser can try his luck again
  • indirect harm like male insects with ejaculate that hardens to form a mating plug that will prevent subsequent males from depositing sperm in the female's sperm receptacle
  • males often establish breeding territories defended against entry by other males and in which the male will have exclusive access to female inhabitants
    • breeding territories represent high-quality habitats with sufficient food and other resources to attract females
  • Mate Guarding - due to sperm precedence (last male to mate gets most of the fertilizations) it may be in the male's interest to guard a mate after mating
    • example comes from a species of fly that lives in the Sonoran Desert, home of the giant saguaro cactus
    • the cacti are sometimes wounded and develop a patch of rotting tissue at the wound that continually leaks fluid that flows slowly down the trunk of the cactus (next time in the desert, look for the evidence of these flows as dried streaks of black gunk below old wounds - they aren't hard to find at all), representing a river of precious water to a species of fly, Odontoloxozus longicornis
      • they get through the hot daytime by cooling themselves through evaporation of fluid drunk from the saguaro river and spend the day with their heads in the river and their abdomens facing away from it, often in two rows up and down the side of the cactus
    • males can mate if they leave off drinking and mount the female, who keeps on drinking
    • after mating, the male can choose to stay and guard the female from subsequent matings by chasing males away
      • this guarding is very costly as the males lose moisture and spend energy to chase other males away
    • males must make a choice to trade off guarding and drinking, a choice you can watch if ever you are walking through a saguaro forest on a hot day
• Competition within the sex for advantage during contests is not a very good explanation of the peacock's tail as it is not of any use in male-to-male contests but arose because of competition among males to be the male chosen by the female

Female Choice

• We have seen (in the section on anisogamy) that there are fundamental reasons for female choice - she has the opportunity to make the choice and fitness consequences result if there are differences among the males in the fitness of the offspring they will produce
• Direct Fitness Effects of mate choice
  • sometimes this benefit is direct and the female will experience the benefit of high-quality males directly
  • G. E. Hill.  1991.  "Plumage coloration is a sexually selected indicator of male quality."  Nature, 350:337-339 - Male house finches (Carpodacus mexicanus) have a red breast, head and rump but the intensity of the color varies.  Brighter colored males are chosen preferentially by females as mates and this paper shows that the brighter colored males bring more food to the nestlings than do the paler males
• Sensory Bias - in some species, choice appears to be triggered by a pre-existing preference, one not linked directly to the males's secondary sexual characters
  • the most famous case of this is the preference of female swordtails - Xiphophorous, a popular fresh water aquarium fish (A. L. Basolo.   1995.  "Phylogenetic evidence for the role of a preexisting bias in sexual selection."  Proceedings of the Royal Society of London, Series B, 265:2223-2228.)
    • the preference for a male swordtail was found in species and genera related to species with sword-tailed males, even though the related species did not have males with swordtails (in fact, some related genera had a stronger preference than did females from species with swordtails)
    • preference arose before swordtails
    • may be related to the phenomenon of a "supernormal stimulus", a stimulus outside of the normal range that provokes increased response
      • the origin of the phenomenon is known but it may be due to the structure of sensory response systems but it is definitely not related directly to females choosing males to promote the fitness of their offspring
• Fisher's Runaway Selection Hypothesis
  • if females choose males for a trait directly beneficial to their offspring, say tail length, then there is selective pressure for males to grow longer tails because they will get more matings than males with shorter tails
    • male tail length may increase, due to directional sexual selection, but eventually reaches a point where natural selection imposes a cost for longer tails
    • however, males that develop shorter tails will never mate, even though their tails are better adapted, as long as females prefer males with longer tails - the trait has come under the control of runaway selection
  • as long as females prefer those long tails, tail length will increase (until heritable variation in tail length is exhausted) and females who mate with long-tailed males will have long-tailed sons that get more matings (this is often called the "sexy son" hypothesis)

• what seems left out of this model is variation in mate choice by females (see assignment)
• Zahavi's Handicap Hypothesis (also known as the Good Genes Hypothesis)
• Fisher assumed that the sexually selected trait was originally beneficial to the female and was the original basis of her choice
• Zahavi postulated that the trait of choice would be a handicap that the male had to bear (A. Zahavi.  1975.  "Mate selection: a selection for a handicap."  Journal of Theoretical Biology, 53:205-214.)
  • the trait had to cost the male in some important aspect of the life history that affected fitness, perhaps lowering the foraging efficiency of the handicap bearer or make him more conspicuous to predators (calling frogs are often attacked by predators that use the call to locate the frog)
    • if males who have the handicap manage to survive and compete for mates, they do so because they have genes that compensate for the cost of the handicap (they have "good genes")
    • the handicap acts as an indicator of the presence of good genes
      • because the handicap is a real cost, it is an honest indicator and prevents cheating by the male as those with bad genes will not be able to produce a competitive handicap trait (their colors will be paler, tails shorter, or calls weaker)
    • A theoretical objection to the handicap/good genes hypothesis is that, over time, heritable variation should be exhausted and females would have little reason for maintaining choice
      • W. D. Hamilton and M. Zuk (1982. "Heritable true fitness and bright birds: a role for parasites?" Science, 218: 384-387.) suggest a solution in that, since parasites can adapt to resistance in hosts, which resistance genes are valuable should be frequency-dependent and, since selection against an allele becomes more positive the closer it gets to a frequency of 0, that this will keep alleles in the population and prevent the loss of genetic variation and keep females choosing because the males with the good genes will change as different parasite genotypes become prevalent
• Studies have supported both Fisher and Zahavi by looking at the crucial difference between the two hypotheses: do the offspring from highly ornamented males have higher fitness than the offspring from less choice males?  Fisher says no and Zahavi predicts yes
  • Studies of stickleback fish, gallinaceous birds, and tree frogs have shown an increase in fitness-related characters for the offspring of preferred mates, supporting Zahavi
  • studies of Drosophila and sand flies have shown a lack of difference, supporting Fisher

Intersexual Conflict and Antagonistic Coevolution

• male and female interest may conflict
• males may rarely mate with the same female twice so, if a male can improve his success at the cost of a female's subsequent ability to bear offspring, it is in his interest to do so but not in the female's interest
  • Haliotis (the abalone) has external fertilization in the coastal water above the rocks on which it lives.  Sperm find, attach to, and penetrate the egg due to protein-protein interactions between surface proteins on both the sperm and egg
    • The first sperm to penetrate the egg gets the mating, so sperm are selected to penetrate the egg surely and quickly
    • eggs penetrated by more than one sperm are not likely to develop successfully, so they are selected for the ability to slow down sperm entry
  • there is a negative effect of mating on female Drosophila
    • they can be stressed by multiple courtships from competing males but a clearer case is the fact that ejaculate often contains some toxic proteins
    • these proteins may lower the viability of competing sperm from previous or subsequent matings by the female but they are also toxic to females, who show lower survivorship and fecundity post mating with toxic males
      • females are selected to resist mating with toxic males or becoming resistant to the toxins
• intersexual conflict, as in the above examples, can lead to antagonistic coevolution, where changes in one sex that improves its mating competitiveness may cause changes in the other sex to resist the original change, which provokes further change in the first sex, which results in further changes in the second sex, and on and on
  • Antagonistic coevolution is also known as an arms race (a term popularized by the armament increases of the West and the Soviet bloc during the cold war)
  • this process can lead to exaggeration of male (and female) traits as the arms race calls for more and more extreme measures to counteract resistance by the other sex

Sex Ratio

• First, we must distinguish between
  • Brood Sex Ratio - ratio, at birth (or hatching, or germination for some plants) of the offspring of a single female.  This is usually consistent with the lifetime sex ratio for offspring from a single female
  • Population Sex Ratio - ratio of males to females in a population of females
• Here, I will use sex ratio to refer to the population sex ratio and always use brood sex ratio when referring to the sex ratio of individual females

Sex Ratio and Sex Determination

Neither the brood  sex ratio nor the population sex ration can be explained exclusively by the species' sex determination mechanism

• the population sex ratio is a weighted average of the brood sex ratios of the individuals comprising the population
• brood sex ratios can vary from the ratio expected from the sex determination mechanism
  • take the XY system - does it produce brood sex ratios that are always 1 to 1? If you assume that meiosis produces 50% Y-carrying sperm and 50% X-carrying sperm, then a brood sex ratio of 1:1 seems a natural result
    • This result depends on at least two more assumptions:
      • Y-carrying sperm are as likely to fertilize eggs as are sperm that carry the X chromosome
      • • We have seen that this is not so (meiotic drive is an extreme example of the differences that can exist between sperm)
      • male zygotes are as likely to survive until birth (hatching, germination) as female zygotes
        • there are many examples known from both animals and plants where sex-linked differences in zygote survival exist, including our species:

        Oscar Riddle. 1927. "Some aspects of sexual difference in prenatal growth and death."  The American Naturalist, 61(673):97-112.

        Abstract:  A first attempt is made to examine three groups of newly developed facts concerning intrauterine fetal life in their relation to sexual difference in prenatal death; the result of this examination is applied to the current conclusion that the mammalian and human male is "inherently weaker than the female." Male and female fetuses are alike forced to undergo their development in a female environment provided by the mother. This condition, combined with the further probable fact that maleness (from the Y-sperm stage to adult life) has tendencies, demands and requirements other and greater than those of femaleness, provides unequal chances to male and female for unrestricted growth and health. An apparently sex-specific hormone (alcohol-soluble; from ovary, placenta, etc.) enters the fetal circulation and is responsible for a special phase of prenatal growth in the uterus of the female; in the mammae and suprarenals (and thyroid?) of both males and females; in the prostate and Mullerian duct system of males. Adverse or antagonistic effects-oedema and degeneration in some cases-have been described in the testes, prostate, penis and epididymis of males. The serological studies in progress at the Frauen-klinik at Halle indicate that the mother's blood reacts to the fetus as to a foreign body. This "antitestis" body probably enters the fetal blood and apparently induces a reaction in the male fetus. The mother's blood does not appear to react similarly against a female fetus. The vitamine B, protein and metabolic requirements in postnatal stages are shown to be unequal in males and females, and this difference is probably present during fetal life. Since these requirements are apparently greater in the male this should result in a higher male death-rate in that fraction of mothers whose nutritional status is near the border line. From the fact that an abnormally high proportion of males is found among the prenatal dead the conclusion is currently drawn by physicians, geneticists and others, that the male is inherently and genetically the weaker sex. This conclusion can be drawn only on the assumption that intrauterine environment is essentially equivalent for male and female. The facts discussed here show that such equivalence does not exist.

        Ralph Catalano, Tim Bruckner, Elizabeth Anderson and Jeffrey B Gould. 2005.  "Fetal death sex ratios: a test of the economic stress hypothesis."  International Journal of Epidemiology, 34(4):944-948

        Abstract:  Background The ratio of male to female live births (i.e. the sex ratio) reportedly falls when populations suffer rare and extreme ambient stressors such as the collapse of national economies. This association has been attributed to the death of male fetuses and to reduced conception of males. We assess the validity of the first of these mechanisms by testing the hypothesis that the fetal death sex ratio varies positively over time with the unemployment rate. Using the unemployment rate also allows us to determine if ambient economic stressors less extreme than collapsing national economies affect the fetal death sex ratio.   Methods We test our hypotheses by applying time-series methods to monthly counts of fetal deaths and the unemployment rate from the state of California beginning January 1989 and ending December 2001. The methods control for trends, seasonal cycles, and other forms of autocorrelation that could induce spurious associations.   Results Results support the fetal death mechanism in that male fetal deaths increased above the values expected from female deaths and from history in months in which the unemployment rate also increased over its expected value.   Conclusions Our findings suggest that ambient stressors as common as increasing unemployment elevate the risk of fetal death among males. We discuss the social, economic, and health costs borne by parents and communities afflicted with these fetal deaths

  • Oh dear!  As a male, I feel a bit beset.  In the first part of this lecture, we asked why there are males at all and now it seems that, although our existence is justified by utility, nature has only grudgingly relented and visits us with travails and afflictions.  Do mothers love their sons less than their daughters?
• In addition, there are sex determination systems with considerable (sometimes total) contributions from environmental conditions (temperature-dependent sex determination in some reptiles is an example).
• So, it appears we cannot turn to sex determination as an explanation of sex ratios.

Fisher's Theory of Sex Ratios

By far, the most common sex ratio is 1 male to 1 female.  Why so?

• Fisher (yes, that Fisher) saw the answer as a type of frequency-dependent selection (although he did not use the term)
• Every generation consists of 50% genes from males and 50% genes from females, no matter what the sex ratio is
  • We must look at fitness over more than one generation, from looking at offspring to looking at grandchildren
• Suppose that two things are true of a population:
  • the sex ratio is not 1 to 1 but is unequal so that there is a rare and a common sex (doesn't matter which sex is rare)
  • there is genetic variation for sex ratio, so that some individuals will inherit the ability to have more males than females, or more females than males, or equal brood ratios
  • Then the population sex ratio will move in the direction of 1:1 (Lets use some simple numbers to illustrate the theory):
    • Suppose the population sex ratio is 1 male to 2 females because all females produce brood sex ratios of 1:2
      • If each female has three offspring, then each male has six offspring because each male must, on average, mate with two females
      • Each female has 3 grandchildren for each of her daughters and 6 for each son or a total of (3 x 2) + (6 x 1) = 12 grandchildren
      • A mutant arises with the ability to produce 2 males for every female
      • The number of grandchildren expected for this individual is (3 x 1) + (6 x 2) = 15 grandchildren
      • If there are no other differences between the mutant and the original sex ratio types, then the mutant allele is favored because it has more offspring in succeeding generations than the original allele
• The mutant allele's advantage is referred to as the Rare Sex Advantage
  • There is a Rare Sex Advantage as long as there is a rare sex
• However, as the allele producing the rare sex (males in our illustration) becomes more common due to its rare sex advantage, the sex favored by the mutation will comprise a greater proportion of the population, so the sex ratio of the population will move towards 1:1
  • When the ratio reaches 1:1, there is no more rare sex and the advantage disappears
    • I do not mean that the brood sex ratios reach 1:1 but that the population consists of a mixture of genotypes produces a 1:1 population sex ratio, even though the brood sex ratios differ from 1:1
  • in our case, a population of 50% original and 50% mutants will produce a population sex ratio of 1:1
• If something happens to alter the sex ratio, subsequent generations will move the sex ratio back towards 1:1, so this an example of a stable equilibrium between the various genotypes for brood sex ratios
• So, the advantage (or disadvantage) of overproducing a sex in one's offspring is related to the frequency of that sex in the population, which makes this a special case of frequency dependent selection

Does Fisher's theory always apply?

Under some circumstances, Fisher's theory will not apply

• Endosymbiosis
• When there is a second genome concerned and that genome resides in the cytoplasm, sex ratios may reflect the interests of both genomes
• The problem for the endosymbiont is that sperm (and pollen) contribute only their nuclei, not their cytoplasm, so the endosymbiont will be transmitted to the next generation only in the cytoplasm of the egg
• These cases usually result in female-biased sex ratios unless there are genotypes of host that are not acceptable to the endosymbiont
• example is Wolbachia, an intracellular bacterium, and terrestrial isopods
• infected populations show little fitness effect (survivorship or fecundity) but are up to 90% female
• bacterium feminizes genetic males by causing the androgenic gland (produces hormones needed to maintain the male phenotype) to atrophy
• (genetic males cured of the bacterium by antibiotics return to the male phenotype in one or two molts after taking the cure)
• Group Selection in Metapopulations
• where there are subpopulations that grow independently of other subpopulations, having more females could make a subpopulation grow more quickly than subpopulations with a 1:1 sex ratio
• when dispersers are sent out, more will come from the larger populations, giving those with more females and advantage
• This is a group selection argument and it is the group that benefits, each subpopulation will experience selection for the rare sex
• Related groups and Individual Selection
  • when groups are related and isolated, a female-biased sex ratio is favored
  • examples are parasitic wasps in which females lay eggs on a host and subsequent parasites that find the infected host choose not to lay their eggs in an already infected host (often, in these wasps, because the first brood has hatched and the larvae will eat anything smaller than them, including the second females later, therefore smaller, larvae) 
    • In these insects, the pupae are often found in the host or near the host's carcass and when the emerge, they mate and the females fly off to find new hosts.  The low density of these flies and their hosts may make it too risky to fly off, find a mate, and then find a host
    • This situation is called Local Mate Competition and when the only males that are competing for mates have the same mother, she will not benefit from the winners, no matter which males or how many they are
  • in this case, all the members of the  group have the same parent that will get all of the female and male genetic contribution to the next generation
  • producing more females increases the number of hosts captured by the next generation
    • the female should produce only enough sons to ensure that all her daughters are inseminated
  • the advantage of producing biased sex ratios accrues directly to the female producing them and so only individual selection is needed to explain this phenomenon
• Care for Offspring and Sex Ratio
  • When the effort needed to produce males differs from the effort needed for females, Fisher's theory applies but to equal effort for each sex, not equal numbers, so more individuals of the less expensive sex will be produced than individuals of the more expensive sex
    • In hymenopteran colonies the production of female offspring is extremely expensive because the mother abandons the hive with a subset of her worker sisters and leaves the nest to her daughter along with its resources and the rest of the workers
    • in this system, males are cheap because they simply fly away to find unmated females and many more males are produced than reproductive females
    • Dennis Hasselquist and Bart Kempenaers.  "Parental care and adaptive brood sex ratio manipulation in birds."
      • Abstract: Under many circumstances, it might be adaptive for parents to bias the investment in offspring in relation to sex. Recently developed molecular techniques that allow sex determination of newly hatched offspring have caused a surge in studies of avian sex allocation. Whether females bias the primary brood sex ratio in relation to factors such as environmental and parental quality is debated. Progress is hampered because the mechanisms for primary sex ratio manipulation are unknown. Moreover, publication bias against nonsignificant results may distort our view of adaptive sex ratio manipulation. Despite this, there is recent experimental evidence for adaptive brood sex ratio manipulation in birds. Parental care is a particularly likely candidate to affect the brood sex ratio because it can have strong direct effects on the fitness of both parents and their offspring. We investigate and make predictions of factors that can be important for adaptive brood sex ratio manipulation under different patterns of parental care. We encourage correlational studies based on sufficiently large data sets to ensure high statistical power, studies identifying and experimentally altering factors with sex-differential fitness effects that may cause brood sex ratio skew, and studies that experimentally manipulate brood sex ratio and investigate fitness effects.
  • Some animal societies (mainly birds but some mammals too), mature but inexperienced individuals are not very likely to successfully reproduce
    • they increase their inclusive fitness by remaining at the nest and helping their mother (or both parents in some species) provide care for younger siblings
      • females are more often found as helpers because males can be more successful earlier and so leave earlier
    • the utility of the helpers varies with the quality of the territory occupied by the parents
      • when the territory is of low quality, what limits offspring production is the fact that the parents can't find enough food to feed the nestlings and helpers further deplete an already short ration of food
      • when the territory is of high quality, what limits offspring production the saturation point for the amount of food a parent can bring back to the nest (it's a type II functional response curve), and helpers can increase the total food supply for the nestlings, increasing the number successfully fledged
    • So, when females are not finding enough food, the sex ratio of broods is shifted toward males because they will not stay in the territory and further deplete food stores
    • When females are finding plenty of food, the sex ratios of broods is shifted toward female production because they will stay and enhance the food supply of subsequent broods
• Haplodiploid Sex Ratios
  • There is one more area of biased sex ratio that we will discuss only briefly, the sex ratio of haplodiploid eusocial insects
• Brood sex ratios may have played an important part in the transition from solitary to social life histories in hymenoptera (all species are haplodiploid)
  • S. A. Frank and B. J. Crespi.  1989.  "Synergism between sib-rearing and sex ratio in Hymenoptera."  Behavioral Ecology and Sociobiology, 24(3):155-162.
  • Abstract.  In many bees and wasps, solitary females produce offspring without help from other females. The transition from lone mothers producing offspring to situations in which females often help to rear siblings is an important step in the origins of complex sociality and nonreproductive castes.  Recent work on Hymenoptera has stressed the role of sex ratio variation in this transition; when a mother's brood is more female biased than average, older daughters are favored to help rear their younger siblings because they are more closely related to sisters than to their own offspring. Here the direction of causality is from biased sex ratios, which arise by some extrinsic mechanism, to the origins of sib-rearing (eusociality). We present a model in which there is a synergism between sib-rearing and female-biased sex ratios, which may either complement the sex ratio variation idea by increasing the rate at which helping spreads or be an alternative hypothesis about the origins of eusociality. The synergism in our model depends on three conditions. 1) Daughters that help cause more food to be provisioned per offspring, which in turn causes larger offspring. 2) Females gain more than males by being large, which favors mothers with helpers to produce a higher proportion of daughters. 3) A helper's inclusive fitness rises as her mother's brood becomes increasingly female biased because a female helper is more closely related to her sisters than to her brothers. A female helper may also be more closely related to her sisters than to her own offspring, but this particular sibling-offspring relatedness asymmetry is not required by the synergism model. These three conditions create a synergism which favors a rapid transition from solitary (subsocial) to eusocial. Demographic and ecological factors that facilitate the evolution of eusociality reduce the stringency of the relatedness asymmetry condition (3) required by our idea. The synergism model therefore complements factors other than relatedness that may have been important during the evolution of eusociality.
• Haplodiploid females are 3/4 genetically identical to their sisters, but only 1/4 identical to their brothers (remember, females share all of their male parent's genes but their brothers have none of their sister's male parent's genes as they have no male parent)
  • This condition leads to what is called Sex Ratio Conflict and was first discussed by Robert Trivers
    • The above situation is not always true but is true if all the workers are offspring of the queen (slavery exists in hymenopteran societies), there is only one queen (some wasps have multiple queens) and if the queen only mated once (some queens multiply mate)
  • Given the above, then there is a potential conflict
    • When reproductive individuals are produced by the colony,  the sex ratio is either under the control of the queen or the workers
      • The queen is equally related to sons and daughters (males will carry only her genes but have only a half complement because of their haploidy) and so should want a 1:1 sex ratio in reproductives
      • the workers are 3/4 related to reproductive sisters but only 1/4 related to males (all of whom are reproductives) and so they should adjust the sex ratio to produce more females than males
    • the empirical evidence supports the workers for colonies that conform to the above assumptions

Is it really the sex ratio at birth that is most important?

There are more males than females born in most human populations.  Boys also have a greater mortality rate.  Is the difference in mortality responsible for the deviation of the birth sex ratio from 1 to 1?

• Let's exaggerate the situation and see if advantage is to be had in this circumstance
• A species of animal has separate sexes and females produce only four offspring in their lifetime.
• Assume that only 50% of males survived to maturity, all females survive, and that the species has a 1:1 brood sex ratio
  • Adult males would have a 2:1 advantage over adult females in contributing to the next generation as, on average, each male will mate with two females, if all females are mated
• A female producing two males and two females would then expect that both female offspring would have her grandchildren and that only one of the males would survive to have her grandchildren, but that he would have twice the number of grandchildren because he mated with two females, for a total of 16 grandchildren
• A female who stopped producing female offspring would then have four male offspring, half of which would die before maturity, giving her two male offspring, each of which mates with two females, for a total of 16 grandchildren

• No, there is no advantage to producing more of the sex with a higher juvenile mortality rate, it is the brood sex ratio (the ratio at birth, by definition) that counts, not the sex ratio of a female's offspring when they reach maturity

  • This is not true if the female who produces more males (in our example) can guarantee that those males will suffer a lower juvenile mortality rate (work it out)

Last updated March 9, 2008