Lecture Notes V: Sexual conflict & selection

Why sex?

Costs of sex:

• Cost of meiosis - 'lose' by sacrificing half the genotype (in comparison to parthenogenic individuals)
• Cost of recombination - sexual reproduction entails the breakup of successful genotypes & the recombination of their elements; recombination may produce new & possibly dangerous homozygosities
• Cost of mating - time & energy to secure a mate + danger of cuckoldry
• Cost of producing males - consider a rare female in a dioecious (having male & female reproductive organs on different individuals) sexual population that reproduces by obligate parthenogenesis. Assuming no reduction in fecundity, the parthenogenetic female is likely to produce twice as many daughters & 4 times as many granddaughters as the average sexual female!

How can sex persist with such costs?

Benefits of sex:

• Genetic hypotheses:
• advantages of recombination (independent of the production of variable offspring, e.g., sexually-reproducing species may have an advantage over asexually-reproducing species in 'clearing' lineage of deleterious mutations)
• Are mutation rates higher where sexually-reproducing species are located?? Insufficient data!
• Ecological hypotheses:
• Hard-selection hypothesis (also known as the lottery hypothesis) - biparental sex is maintained by unpredictable changes in the environment; 'variable' offspring may be better able to survive in the 'new' environment
• Soft-selection hypothesis - sex is maintained by intraspecific competition in a stable environment, i.e., production of variable or 'rare' offspring reduces competition for resources
• Red Queen hypothesis - sex is maintained by selection resulting from interactions between biological 'enemies' (e.g., hosts & parasites); outcrossing & recombination favored because they allow production of 'rare' offspring expected to have a greater chance of 'escaping' parasites

Why sexes?

Imagine a population with sexual reproduction, but without sexes. Also, there is a range of parental gamete types:

• Small - 'inexpensive' to produce (energetically)
• Intermediate - too large to produce in great numbers BUT too small to support development of embryo without additional cytoplasm
• Large - energetically expensive but with sufficient cytoplasm for development

Such variation might lead to ‘specialization':

• Small gametes - specialize in seeking out larger gametes & would 'compete' with other small gametes
• Large gametes - no need to seek additional cytoplasm; 'specialize' in containing necessary nutrients

This model is hypothetical & other explanations are possible, but given the existence of males and females, how can an individual male (sperm-maker) or female (egg-maker) maximize their fitness?

• Females - have more invested in each gamete than do males, e.g., bird eggs may constitute 25% or more of a female's body weight and, while the eggs of female mammals are smaller, females produce the placenta, nourish the embryo(s), & produce milk after birth
• Males - individually, sperm are relatively inexpensive to produce

Observational evidence:

• Reproductive success in male & female Jamaican Lizards (Anolis garmani; Trivers 1972):

Variance is much greater for male lizards.

Source: http://www.naturalhistorymall.com/Herp%20Lists/saurialist.html

• Bateman, A.J. 1948. Intrasexual selection in Drosophila. Heredity 2:349-368.

Again, variance in male reproductive success is much greater than for females.

Male & female investment in reproduction (Trivers 1972):

Parental investment = any behavior toward offspring that increases the chances of the offspring's survival at the cost of the parent's ability to invest in future offspring.

• Males & females - both selected for producing the number of offspring that results in maximum reproductive success
• Reproductive success = not measured simply by number of offspring but by difference between number of offspring (benefits) & decreased reproductive potential in the future because of present offspring (costs)
• Females often invest more in each offspring & their investment curve tends to rise more quickly (shown below). As a result, males & females may disagree about the optimum number of offspring &, as a result, males in many species will seek access to additional females. Such behavior leads to greater competition & selection.

Source: Barash 1982 (Figure 10.3, p. 219)

Male-male competition & sexual selection

• R.L. Trivers suggested that sexual selection will act primarily on the sex investing less (males) & individuals of this sex will compete with each other for access to the sex investing more (females)
• Sexual selection = operates through variance in reproductive success; usually acts more strongly on males because males experience greater variance in reproductive success

Variation in reproductive success among men & women in two Xavante Indian villages
in Brazil (Salzano et al. 1967).

• Charles Darwin - suggested that sexual selection would lead to the evolution of two sorts of male characters:
• Intrasexual selection - leads to evolution of characters involved in 'winning' in 'combat' with other males
• Intersexual selection = epigamic selection - leads to evolution of characters important in attracting females

• Pre-mating mechanism:

Examples:

Thornhill, R. 1980. Sexual selection within mating swarms of the lovebug, Plecia nearctica. Anim. Behav. 28:405-412.

• Males emerge from litter & hover in swarms sometimes consisting of thousands of individuals.
• Females fly into swarms & are quickly grasped by a hovering male.
• Females - always enter swarms from below, so . . .
• Males - those near the bottom of swarms have greater mating success

• Hovering males frequently fly into or toward ‘neighbors' ---> Such interactions lead to stratification of male swarms by size

Sexual coercion in a terrestrial salamander: males punish socially polyandrous female partners (Jaeger et al. 2002) - Traditionally, the theory of sexual selection has been divided into two components: intrasexual competition for mates and intersexual mate choice. Clutton-Brock and Parker (1995) suggested that sexual coercion be included in the sexual selection theory. Sexual coercion can be defined as a means by which males attempt to manipulate females into mating with them. Jaeger et al. (2002) examined the concept of sexual coercion in Plethodon cinerus, red-backed salamander. They found that males aggressively punished socially polyandrous female partners more severely that socially monogamous female partners. Males spent more time in the threat posture (ATR) and displayed more edge behavior (escape behavior) when associated with a socially polyandrous female partner. Males spent less time touching a socially polyandrous female partner. Males, on average, kept a greater distance between himself and a socially polyandrous female partner. Males also bit socially polyandrous female partners with significantly greater frequency than socially monogamous female partners. This data supports the hypothesis that greater male aggression will be displayed towards a socially polyandrous female partner than towards a socially monogamous female partner.                                                                                                   - Contributed by Jodi Stacy

Correlation between polygyny & sexual dimorphism

In polygynous species, one male mates with several females &, as a result, male variance in reproductive success increases. Increased variance ---> increased intrasexual selection ---> increased selection for increased size & strength

Relationship between degree of polygyny (mean harem size) & sexual dimorphism in primates (from Barash 1982; based on data from Alexander et al. 1979).

Pre- & post-mating strategies

1) Abele, H. & S. Gilchrist. 1977. Homosexual rape and sexual selection in acanthocephalan worms. Science 197:81-83

• Parasitic worms that occur in intestines of many mammals
• After mating with a female ---> male introduces a copulatory plug that prevents his sperm from leaking out & prevents other males from copulating with the female
• When a male encounters another male ---> introduces a plug but no sperm which renders the 'victim' sterile

• after mating, male mosquitoes secrete a hormone that reduces the sexual receptivity of the must-mated female

• transfers sperm AND removes sperm deposited by 'preceding' male (see photo to the right)

• male bedbugs (Afrocimex spp.) possess structures that mimic female genitalia; rival males who mount these female 'mimics' waste their sperm

• many species exhibit prolonged copulation (a form of mate guarding)

Enallagma exsulans in copula

6) Hrdy, S.B. 1974. Folia Primatol. 22:19-58 (langurs) & Bertram, B.C.R. 1976. In: Growing points in Ethology. Cambridge Univ. Press (lions)

• male langurs & lions practive infanticide after taking over a troop or pride to bring females into estrus sooner

• males use prey in courtship ---> offers prey to a female, then (if she accepts) mates with her
• male strategies:

• some steal prey from other males ('victims' must wait longer before copulating)
• deceptive transvestism - some males act like females (landing near another male that has a prey item & lowering wings as receptive females do) to obtain a prey item

Intersexual selection & mate choice

Mate choice:

• mechanism by which intersexual selection operates
• any pattern of behavior, shown by members of one sex, that leads to their being more likely to mate with certain members of the opposite sex than with others
• Criteria on which mate choice may be based:

I - Choice for high fecundity or fertility - in many species, females continue to grow after reaching sexual maturity & larger females can often produce more eggs & offspring

• Male choice for larger females, e.g., isopods (below, left; Behaviour 55:1-14), Mormon crickets (below, right) (Gwynne 1981), & checkered white butterflies (Anim. Behav. 30:108-112)

Female Isopod (Arcturus hastiger) with children on antenna

Mormon cricket

 
• Female choice for males with increased fecundity, e.g., females may select males that court most vigorously, if 'vigor' is correlated with sperm supply

Smooth newt (Triturus vulgaris) - males deposit spermatophores on bottom of ponds during sexual encounters &, the more spermatophores deposited, the greater the probability that a female will pick up a male's spermatophore(s)

II - Choice for immediate gains and/or parental ability

• Males in many species provide females with food as

a necessary prelude to mating

• Females tend to accept only males with insect prey above a certain size. Possible benefits of such a preference:
• Male mates while female eats. A larger insect means that females eat longer and, therefore, copulations are longer & this helps ensure fertilization of eggs

• More food from a male means less hunting by the female; less hunting means a reduced risk of being caught in a spider's web
• Males that bring larger prey may be of higher quality

1 - Food given to females may contribute to reproductive success by providing energy at a critical time

2 - Feeding may strengthen the pair bond (possibly true but difficult to test!)

• Females may not associate with males who feed them at low rates
• Females may divorce males who do not provide sufficient food
• Among species in which males provide some or all of the parental care, females may choose males on basis of capacity to do so
• Avian courtship feeding - ability to feed female may be correlated with ability to feed young

• Dilution effect - more eggs in the nest means reduced chance that particular eggs will to lost to predation
• Males are more vigorous in keeping other fish from a nest during the 'parental phase' than during the 'courtship phase' ---> female laying eggs in nests with eggs are likely to be mating with 'parental phase' males

III - Choice for mate complementarity

• Reproductive success may be affected not only by various individual qualities but also by the extent to which a pair's genotypes & capacities to provide reproductive effort complement one another

• Deleterious genes more likely to be expressed
• Offspring insufficiently variable to cope with varying environment
• Beneficial interactions between different alleles (heterosis) at same genetic locus lost
• Offspring more alike &, as a result, may compete more intensely

However, outbreeding also has potential 'costs':

• Genes adapted for particular environment may be lost or suppressed
• Travelling to another population (dispersal) may be costly & dangerous
• Infections from pathogens carried by mate more likely

• Prior to mating, members of one sex move away from the area where hatched or born (natal dispersal):

• Birds ---> females usually disperse
• Mammals ---> males usually disperse

• Recognition of kin . . . if so, how?:

• Proximity
• Early experience (i.e., learn characteristics of close kin)
• Phenotype matching
• Innate recognition
• For more information, click here and/or here!

• Optimal discrepancy hypothesis:

Tests of model:

• Bateson, P. 1982. Nature 295:236-237.

• McGregor & Krebs (1982):

How might such preferences be generated? Perhaps the result of an interaction between imprinting & habituation:

• Sexual imprinting
• animal forms social attachment to another animal or object (sexual attachments formed during 'critical period')
• reduces responsiveness to the 'novel'
• Habituation - repetitive 'stimulation' reduces responsiveness to the 'familiar'

• Combination of these two processes (sexual imprinting & habituation) could lead to a preference for mates a bit different from the 'familiar.'

Choice for complementarity in reproductive effort ---> especially important in species where the pair bond is maintained over several breeding seasons

Coulson (1966) - Kittiwakes (Rissa tridactyla)

• Newly-formed pairs with little breeding success ---> divorce
• Newly-formed pairs with greater breeding success ---> tend to remain together & breeding success tends to improve in subsequent years

• Why do experienced pairs have greater breeding success?
• Advantages due to age or experience:
• older birds tend to lay more eggs & breed earlier
• increased duration of a pair bond = earlier laying dates
• older birds = more efficient at feeding young
• Quality of nest sites - younger birds may have to nest in peripheral locations or in lower quality territories
• Time saved by mating with a familiar partner, e.g., less courtship needed = earlier breeding = more time for additional broods and/or better choice of nest sites (in colonial species)

IV - Choice for good genes (i.e., genes that increase the ability of offspring to survive, compete, & reproduce)

• Fisher (1930):
• Elaborate male displays may be sexually selected because they make males attractive to females. But, how could such preferences develop &, thereafter, be maintained?
• Initial preference ---> perhaps because a particular trait was correlated with male quality (e.g. a longer tail = better flyer) or simply made males easier to locate or detect
• Association or covariance important ---> if male preferences have a genetic basis, the advantage is passed on to a female's sons AND genes that cause females to prefer that trait will also be favored ----> POSITIVE FEEDBACK = RUNAWAY SELECTION!

• Long-tailed Widowbirds (Euplectes progne) - polygynous species that occupies open savannah habitats in Africa

(a) No difference among four groups before tail length was altered. (b) After tails were altered, mating success declined for males with shortened tails and increased for males with elongated tails. Mating success = number of active nests in a male's territory (Figure from Krebs and Davies 1993; Fig. 8.7, p.191)

Long-tailed Widowbird photograph  by Steve Wilson

• Zahavi (1975) - The Handicap Hypothesis:
• conspicuous male characters represent a 'handicap' because such characters may actually reduce a male's capacity to survive
• females selecting 'handicapped' males, therefore, are selecting mates with a demonstrated ability to survive in spite of their handicap (i.e., must be good quality males)
• could ‘work' if 'handicaps' are flexible or condition dependent
• For more information, check out this site:

• Kodric-Brown & Brown (1984):
• Selection favors evolution of phenotypic traits that vary in such a way that their expression is highly correlated with genetic fitness.

Graphical model of sexual selection by truth in advertising. The model assumes
that both expression of the sexual characteristic and overall fitness are quantitative
traits, distributed normally among males. If there is a significant positive covariance
between these two variables, females that mate with males with extreme expression
of the sexual trait will be choosing individuals of superior overall genetic quality (shaded area)
(from Kodric-Brown and Brown 1984).

• Advantage to females choosing males of high fitness will:
• Favor evolution of male traits that maintain a high correlation between phenotypic expression & genetic quality
• Favor evolution of females that exhibit discrimination in choice of mates
• Predictions or consequences of the Truth in Advertising model:
• Sexually selected traits ---> highly correlated with phenotypic vigor & components of fitness like growth rate, predator avoidance, disease- & parasite-resistance, & competitive ability
• Traits ---> costly (expression requires expenditure of limited energy that could be allocated to other structures & functions
• Genotype-environment interactions should enhance effect of sexual selection & contribute significantly to observed variation among males in sexual traits
• Fitness of both male & female offspring should be positively correlated with degree of 'expression' in father
• Many organisms:
• Both male-male competition & female choice important in sexual selection, & same traits should often be employed in both intermale contests & courtship
• Use of traits in contests with other males helps maintain 'honesty'
• When several traits are important in sexual selection, expression should be highly correlated among males
• Exaggerated male traits ---> may aid in intraspecific competition for limited resources like food & shelter

• Important point ---> Traits that advertise male genetic quality need not reflect a trade-off between enhanced reproductive success and reduced survival (i.e., need not be 'handicaps' in the sense of Zahavi)

CONCLUSION ---> Choice for good genes?? Probably . . . as long as 'genes' are expressed in a condition-dependent manner

V - Choice for resources and/or high status

Where one sex possesses resources necessary for reproductive success, individuals of the other sex may show preferences based on quality of resources.

Experimental evidence:

Wells (1977) - Green frogs (Rana clamitans)

• Females chose males with territories that contain dense vegetation in which to lay eggs

• Females tend to choose males with territories in which bee nests are located (feed preferentially on honey & larvae in such nests)

Jones (1981) - Wrasse (Pseudolabrus celidotus)

Females tend to choose males with territories in deeper water where eggs are most safe from predators

Choice for high status ---> Advantages:

• Immediate - able to mate without interruption by other males
• Progeny may benefit from father's high status through greater parental care & protection
• Possible genetic advantage - provided that a male's ability to assume high status has some genetic basis

• Breed et al. (1980) - Cockroaches (Nauphoeta cinerea)
• Dominant males mate more often than subordinate males because:
• dominant males are more active & encounter females more frequently
• Females are able to discriminate between dominant & subordinate males by odor

• Cox & LeBoeuf (1977):
• Elephant seal (Mirounga angustirostris) - Females more likely to make a vocal protest when mounted by a low-ranking male & such protests attract other males who attempt to displace him
• Net effect = makes mating by dominant males more likely

• West et al. (1981) - Brown-headed Cowbird (Molothrus ater)
• Females induced to solicit copulation by male song & dominant males sing more 'potent' songs than subordinates
• Why sing a less potent song? Dominant males attack submissive males that sing 'potent' songs (isolated males will develop more potent songs)

Strategies of female mate choice

Given: Females may base choice on one, or some combination, of the aforementioned characteristics (e.g., fecundity, parental ability, complementarity, good genes, resources, and high status).

Questions:

• How does a female find the best possible male?
• How long should a female search?
• Should males be judged against a fixed standard or by relative criteria?

• Time - females limited by last date at which they can initiate breeding & still be maximally successful; this will limit the number of males they can evaluate
• Mobility - Females may not be able to transverse habitat easily enough to find all available males
• population may be fragmented into subpopulations isolated by unsuitable habitat
• other potential barriers, e.g., currents (fish), predators, & strong prevailing winds (flying insects)
• Memory - probably only 1 or a few males can be remembered at any one time, & none for very long

A Possible Model for Female Mate Choice (Janetos 1980):

Assumptions:

• Females mate only once
• Males may mate more than once & a male's fitness does not decline as he accumulates mates
• Males are dispersed in space such that they are encountered randomly with respect to fitness
• Males cannot predict where & when a female will arrive
• Males are unable to manipulate one another or females to increase chance of mating
• Fitness of males ranges from 0 to 1 (mean = 0.5)

Possible female strategies:

• Random mating
• female mates w/ first male encountered
• little time & movement & no memory required
• average fitness of male chose will, on average, be same as population mean
• Fixed standard
• Judge males against a fixed standard & choose 1st one above that (but can't go back to previous males)
• Females choose only males above 'fitness standard' UNTIL they run out of time ---> then must choose next available male (i.e., choose randomly)
• One-step decision process
• Females initially have high standard that is gradually relaxed as they run out of time (& can't go back to previous males)
• Females should only mate & end search if male on hand is better than they could expect to find by continuing to search (until they run out of time)
• Best-of-n-males
• rank males on relative basis & choose the best
• requires memory of male quality & locations & mobility (to return to previously encountered male)

RESULTS:

• How many males should a female examine?
• Benefit = fitness of male ---> negatively accelerating function for all options
• Costs:
• Risk of predation during search
• Searching requires energy that could be used to produce or nourish young
• Time - may get too late to successfully raise young

So, COST = SOME INCREASING FUNCTION OF n (no. of males examined)

The expected fitness of males chosen by each strategy as a function of n, the
number of males that the female can encounter. Male fitness is described by
a uniform distribution on the interval [0, 1] (Janetos 1980).

Value of model:

• Probably cannot be applied completely to living species (because of false assumptions)
• Shows the constraints on female behavior & shows that even simple forms of female choice can yield large benefits

Literature Cited:

Alexander, R.D., J. Hoogland, R. Howard, K. Noonan, and P. Sherman. 1979. Sexual dimorphism and breeding systems in pinnipeds, ungulates, primates, and humans. In Evolutionary biology and human social behavior (N. Chagnon and W. Irons, eds.). Duxbury, N. Scituate, MA.

Andersson, M. 1982. Female choice selects for extreme tail length in a widowbird. Nature 299:818-820.

Barash, D.P. 1982. Sociobiology and behavior, second ed. Elsevier, New York.

Bateson, P. P. G. 1980. Optimal outbreeding and the development of sexual preferences in Japanese quail. Zeitschrift fur Tierpsychologie 53: 231-244.

Beecher, M. & I. Beecher. 1979. Sociobiology of Bank Swallows: reproductive strategy of the male. Science 205:1282-1285.

Breed, M.D., S. Smith, & B.G. Gall. 1980. Systems of mate selection in a cockroach with male dominance hierarchies. Anim. Behav. 28:130-134.

Clutton-Brock, T. H. and G.A. Parker. 1995. Sexual coercion in animal societies. Animal Behaviour 49:1345-1365.

Coulson, J.C. 1966. The influence of the pair-bond on the breeding biology of the Kittiwake gull. J. Anim. Ecol. 35:269-279.

Cox, C.R. & B.J. LeBoeuf. 1977. Female incitation of male competition: a mechanism in sexual selection. Am. Nat. 111:317-335.

Craig, G. 1967. Mosquitos: female monogamy induced by male accessory gland substance. Science 156:1499-1501.

Cronin, E.W., Jr. and P.W. Sherman. 1976. A resource-based mating system: the Orange-rumped Honeyguide. Living Bird 15:5-32

Fisher, R.A. 1930. The genetical theory of natural selection. Clarendon Press, Oxford.

Gwynne, D.T. 1981. Sexual difference theory: Mormon crickets (Anabrus simplex) show role reversal in mate choice. Science 213: 779-780.

Halliday, T. R. 1976. The libidinous newt.  An analysis of variations in the sexual behaviour of the male smooth newt. Animal Behavior 24:98-414.

Jaeger, R.G., J.R. Gillette, and R.C. Cooper. 2002. Sexual coercion in a terrestrial salamander: males punish socially polyandrous female partners. Animal Behavior 63: 871-877.

Janetos, A.C. 1980. Strategies of female mate choice: a theoretical analysis. Behav. Ecol. Sociobiol. 7:107-112.

Jones, G. P. 1981. Spawning-site choice by female Pseudolabrus celidotus (Pisces: Labridae) and its influence on the mating system.
Behav. Ecol. Sociobiol. 8:129-142.

Kodric-Brown, A. and J.H. Brown. 1984. Truth in advertising: the kinds of traits favored by sexual selection. American Naturalist 124:309-323.

Krebs, J.R. and N.B. Davies. 1993. An introduction to behavioural ecology, third edition. Blackwell Scientific Publications, London.

McGregor, P.K. & J. R. Krebs. 1982. Mating and song types in the Great Tit. Nature 297:60-61.

Ridley, M. and C. Rechten. 1981. Female sticklebacks prefer to spawn with males whose nests contain eggs. Behaviour 76:152-161.

Salzano, F.M., J.V. Neel, and D. Maybury-Lewis. 1967. Further studies on the Xavante Indians. I. Demographic data on two additional villages: genetic structure of the tribes. Amer. J. Human Genetics 19:463-489.

Thornhill, R. 1976. Sexual selection and nuptial feeding behavior in Bittacus apicalis (Insecta: Mecoptera). American Naturalist 110:529-548.

Thornhill, R. 1979. Adaptive female-mimicking behavior in a scorpionfly. Science 205:412-415.

Trivers, R.L. 1972. Parental investment & sexual selection. Pp. 136-179 in Sexual selection and the descent of man (B. Campbell, ed.). Aldine, Chicago.

Waage, J. 1979. Dual function of the damselfly penis: sperm removal and transfer. Science 203:916-918.

Wells, K.D. 1977. Territoriality and male mating success in the green frog (Rana clamitans).  Ecology 58:750-762.

West, M.J., A.P. King, and D.H. Eastzer. 1981. Validating the female bioassay of cowbird song: relating differences in song potency to mating success. Anim. Behav. 29:490-501.

Zahavi, A. 1975. Mate selection - a selection for a handicap. J. theor. Biol. 53:205-214.

Related, & interesting, links:

Advantage of Sex

Sexual Selection in Birds

Sexual Selection and the Biology of Beauty

Evolution of Sex and Sexual Selection

Female Sexual Selection: Part 1

Female Sexual Selection: Part 2

Mate Choice

Mating Systems & Parental Care

Neoteny and Two-way Sexual Selection in Human Evolution

Hidden Biases and Sexual Selection

Sex and Sex Ratios

Sex is best when you lose your head

Why are there only two sexes?

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