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 urchin cow

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 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 and 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)

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 bias Male courtship in the water mite Neumania papillator: male leg trembling exploits female sensory bias female 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 average value for the sons and daughters of a male. Males with longer- stalked sons should have daughters with longer-stalked 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 results Females from lines selected for longer male eyestalks more often preferred long- stalked males Females from lines selected for shorter male eyestalks more often preferred shorter-stalked males

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