sexual selection. from wildlife of pakistan fundamental asymmetry of the sexes: anisogamy image from...
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Sexual selection
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From Wildlife of Pakistan
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Fundamental asymmetry of the sexes: anisogamy
image from W. Lennarz
sea urchin sperm is 1/10,000th the size of the egg
sea urchincow
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Isogamy is much rarer
• Isogamy
– single-celled flagellates
• Anisogamy (with motile eggs)
– “primitive” multicellular organisms
• Oogamy (anisogamy with non-motile eggs)
– virtually all other multicellular plants, animals, fungi
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Chlamydomonas isogametes mating
image from Visions Unlimited image from U. Goodenough
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The fundamental asymmetry of the sexes
• Males produce many small, energetically cheap sperm
• Females produce few large, expensive eggs
– Males should maximize sperm output, number of fertilizations, and will compete for them
– Females should maximize success of each egg, they should choose mates, provide nutrition and care for young
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This basic asymmetry drives sexual dimorphism
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Bateman’s principle• male reproductive success is limited by
access to mates– males should maximize opportunities for
fertilizations, without discrimination– they should compete for mates
• female reproductive success is limited by their ability to provide nutrition to eggs and embryos– females should be choosy
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Asymmetric limits on reproductive success of males and females
• A.J. Bateman’s (1948) classic test in Drosophila
• 24 populations, each with 3 males and 3 females
– each male and female had exactly 3 potential mates
– each was “marked” with a dominant mutation
• he could determine who mated with whom and how many times
• he could count offspring produced
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Field studies of Bateman’s principle• Jones, Arguelo and Arnold (2002) collected
eggs from adult rough-skinned newts after they had mated
• they used paternity analysis to determine fathers of all young hatched
– they could determine the number of mates and the number of offspring for all adults
photo by W. Leonard
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Most males failed to mate
And left no offspring
a few big winners
all females mated at least once
and showed much less variation in reproductive success
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consistent with Bateman’s principle, male reproductive success increased greatly with the number of mates
for females, less so
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Figure 10.35. Lifetime reproductive success in elephant seals
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Sexual selection should be much stronger on males of most species
• it arises from 2 sources:
– male-male competition or intrasexual selection
– female choice or intersexual selection
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Male-male competition
• often strongest where males can monopolize females
• or e.g. in highly territorial species where males control access to nest sites or feeding territories
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Male-male competition: combat for mating territories in marine iguanas• Galápagos Island iguanas
Amblyrhynchus cristatus graze algae
• they have no predators and do not compete for food– natural selection on body size is
stabilizing– the largest individuals cannot feed
enough to support metabolic costs
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Natural selection favors intermediate size, but males often exceed this
* largest size of no weight loss in 91-92 and 92-93
from Wikelski and Trillmich (1997)
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So why are male marine iguanas so large?
large males command the best mating territories
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Mating territories on Camaaño Islet, Galápagos
Male 59 was the largest male and won many battles for his preferred territory. He gained most of the copulations.
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Adaptations to male-male competition
alternative male mating strategies
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Alternative male mating strategies
• bluehead wrasse (and many other coral reef fishes): territorial males pair spawn with females
• they expend considerable energy on gaining and defending territories
• “sneaker” males join spawning rushes, and release sperm simultaneously
territorial male
female
photo by R. Warner
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Horseshoe crabs
Attached males ride females to shore, and release sperm as the female lays eggs (“pseudocopulation”).
Satellite males wedge under the carapace of an attached male and release sperm while it spawns.
While satellite males are often older, more feeble males, paternity analysis shows they gain many fertilizations.
attached male
satellite male
female
photo by J. Brockmann
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Sperm competition: competition that occurs after mating between sperm of > 1 male
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Sperm competition has favored many adaptations in male insects
In damselflies, the second male to mate uses barbed penis to dislodge sperm from an earlier male
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Female choice
• often occurs when males cannot monopolize females
• males advertise for mates
• has led to the most elaborate courtship behaviors and male secondary sexual characters
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Female choice in barn swallows• Hirundo rustica breeds in large
colonies in Denmark
• Monogamous (except for cheating); males help care for young
• Male and female investment in offspring are ~ equal
– expect little or no sexual dimorphism
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Female choice in barn swallows
• But male behaviors suggest otherwise ...
– males establish small breeding territories
– then they display to attract mates
– when they do, the trait they “show off” is their tail
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And tail length is sexually dimorphic
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Classic experiments of Anders Møller (1988) showed female choice for longer tails
• He shortened and lengthened tails on 4 groups of banded birds
(1) tails shortened(2) tails clipped and reattached(3) tails unaltered(4) tails elongated
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Classic experiments of Anders Møller (1988) showed female choice for longer tails
• He released them back into the colony and scored:
– time required to attract a mate
– the per cent of second clutches
– the number of fledglings sired
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The results show:
(1) females are choosy
(2) female choice favors longer tails
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Why are females so choosy?
• good genes
• males provide a resource that varies in quality
• females respond to a cue, unrelated to mating, that males exploit (sensory bias)
• runaway sexual selection
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Choosy females get good genes in tree frogs
• Males of the eastern US grey tree frog, Hyala versicolor, call to attract mates
• Field observations by Gerhardt and colleagues suggested female choice for calls– males sing longer calls when other males are
present– females will pass chorusing males to mate with
males farther away
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Females choose longer calls in the lab
they approach calls with longer “trills,” even when shorter call is louder
they pass by a speaker playing short calls to approach a longer call, farther away
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Welch et al. (1998) showed that long-calling males have better genes!
they collected eggs from field-caught females
eggs fertilized by sperm from long-calling and short-calling males
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• maternal half-sibs compared for several fitness traits
– growth
– time and size at metamorphosis
– survival
Results
10 comparisons, no difference
8 comparisons, offspring of long-callers better
0 comparisons, offspring of short-callers better
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Female choice for resources in hangingflies
• Bitticus apicalis males present a “nuptial gift” of food to females
• females copulate for longer periods with males that present larger gifts
• the longer she copulates, the more sperm he transfers
Photo ©2005 S. Nance
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female choice: longer matings with males bearing bigger gifts
from R. Thornhill (1976)
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from R. Thornhill (1976)
the payoff to the male is an increased quantity of sperm transferred
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if she finishes eating before 20 minutes, she flies off for another male (and meal)
if food is left after 20 minutes, the male gets a doggie bag
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Why are females so choosy?• good genes
• males provide a resource that varies in quality
• females respond to a cue, unrelated to mating, that males exploit (sensory bias)
• choice is arbitrary (as in runaway sexual selection)
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The sensory bias hypothesis
• females evolve acute responses to cues used in foraging, predator avoidance, or species recognition
• males exploit these sensory “biases” and display the cues (often exaggerated) that females choose
• these cues have nothing to do with mating per se, nor do they signal differences in male quality
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Sensory biasMale courtship in the water mite
Neumania papillator: male leg
trembling exploits female sensory biasfemale in net-stance
male is leg-trembling
Females respond to the frequency
produced by swimming copepods,
and male leg trembling produces
this same frequency
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the male is now fanning water past the spermatophores, which the female may pick up
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Evidence for sensory bias
• male leg trembling “mimics” the frequency produced by copepod swimming
• female “clutching” behavior in response to males resembles that used while females hunt
• hungry females respond more often to male water mites than fed females
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Phylogenetic evidence
• critical proof: the female preference (presence of net-stance behavior) evolved prior to the male trait (leg trembling)
this phylogeny shows that net-stance evolved before trembling
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Phylogenetic evidence for sensory bias
• but an equally likely hypothesis leaves their order of appearance unresolved
Proctor favors sensory bias as the best explanation, given the weight of the phylogenetic and behavioral evidence
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Female choice may be arbitrary• an initial arbitrary preference by
females for a male trait leads to an automatic “runaway process”– the sexy-son hypothesis
• females show an arbitrary preference for a male trait
• those females with stronger preference will give birth to sons that themselves would be more preferred
• this process will create exaggerated male traits
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Female choice may be arbitrary
• the “runaway sexual selection hypothesis” is a more formal, complex formulation of this sexy-son idea
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Sexual selection in stalk-eyed flies
• Malaysian flies with eyes on long stalks—males of similar size have much longer eyestalks than females
• males with longer eyestalks – win contests for “roosting” areas– are chosen by females
Photo by J. Wilkinson
Photo from Univ. College of London
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Runaway selection in stalk-eyed flies?
Photo from Univ. College of London
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Each point is the Each point is the average value for the average value for the sons and daughters of sons and daughters of a male. a male.
Males with longer-Males with longer-stalked sons should stalked sons should have daughters with have daughters with longer-stalked longer-stalked preferences.preferences.
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The prediction
If we select longer-stalked males as breeders, their daughters will prefer longer eyestalks.
This will set up a self-reinforcing “loop,” or runaway sexual selection.
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Wilkinson and Reillo’s (1994) experimental design
• 3 lines established from Malaysian natural population
– control: 10 random males X 25 females– long-selected: 10 longest-stalked males X 25 females– short-selected: 10-shortest-stalked males X 25 females
• this was done each generation for 13 generations
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Wilkinson and Reillo’s (1994) experimental design
• paired tests of female choice in females from each selected line:– one shorter and one longer-stalked male
placed in center of chamber
– 5 females added
– scored the number of times females chose to “roost” with the short vs. long-stalked males
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The resultsFemales from lines Females from lines selected for selected for longer longer male eyestalksmale eyestalks more more often preferred long-often preferred long-stalked malesstalked males
Females from lines Females from lines selected for shorter selected for shorter male eyestalks more male eyestalks more often preferred often preferred shorter-stalked shorter-stalked malesmales
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Implications
• stalk-eyed fly females are choosy
• eyestalk length and female preferences are
both heritable
• selection on male traits produced a correlated
response in female preference!
• due to genetic correlations between trait and
preference, runaway selection can happen
Photo by J. Wilkinson