Sexual selection

From Wildlife of Pakistan

Fundamental asymmetry of the sexes: anisogamy

image from W. Lennarz

sea urchin sperm is 1/10,000th the size of the egg

sea urchincow

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

Chlamydomonas isogametes mating

image from Visions Unlimited image from U. Goodenough

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

This basic asymmetry drives sexual dimorphism

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

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

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

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

consistent with Bateman’s principle, male reproductive success increased greatly with the number of mates

for females, less so

Figure 10.35. Lifetime reproductive success in elephant seals

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

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

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

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)

So why are male marine iguanas so large?

large males command the best mating territories

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.

Adaptations to male-male competition

alternative male mating strategies

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

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

Sperm competition: competition that occurs after mating between sperm of > 1 male

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

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

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

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

And tail length is sexually dimorphic

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

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

The results show:

(1) females are choosy

(2) female choice favors longer tails

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

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

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

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

• 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

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

female choice: longer matings with males bearing bigger gifts

from R. Thornhill (1976)

from R. Thornhill (1976)

the payoff to the male is an increased quantity of sperm transferred

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

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)

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

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

the male is now fanning water past the spermatophores, which the female may pick up

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

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

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

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

Female choice may be arbitrary

• the “runaway sexual selection hypothesis” is a more formal, complex formulation of this sexy-son idea

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

Runaway selection in stalk-eyed flies?

Photo from Univ. College of London

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.

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.

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

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

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

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