Sexual Selection and Courtship Behavior in Insects

5/24/10
Sexual Selection
and Courtship
Behavior in
Insects
Jennifer M. Gleason
jgleason@ku.edu
Assistant Professor
(Associate Professor starting 8/10)
Ecology and Evolutionary Biology
University of Kansas
Outline
• Background
– Evolutionary definitions
– Sexual dimorphism
– Parental investment
• Sexual selection
– Intrasexual selection
– Intersexual selection
• Sex role reversal
• Courtship evolution in Drosophila
1
Adaptation
• Biological process
• Organism becomes better suited
to its environment
– Fitness
• Shaped by natural selection
• Occurs over geological time
(hundreds to thousands of
generations)
http://www.time.com/time/photogallery/0,29307,1844904_1772238,00.html
Fitness
• Capacity to produce lots of
offspring relative to other
individuals
• Survive longer than other
individuals (and consequently
leave more offspring)
2
Natural Selection
• Heritable
– Trait must be passed from parent to offspring
– Genetics
• Variable
– Within a species the trait must vary
– Different individuals have different traits
• Differential fitness
– The trait must be advantageous for some individuals
• Differential fitness is nonrandom
– All individuals with displaying one form of a trait do better than
individuals displaying an alternate form of the trait
Insect Life Cycles
Holometabolism: complete metamorphosis
3
Insect Life Cycles
Egg
Nymph
(many molts)
Adult
Hemimetabolism: incomplete metamorphosis
4
Sexual Dimorphism
• Males and females
differ in size,
appearance and/or
behavior
Ischnura damselflies
Orgyia recens
Male
Female
5
Chalcosoma caucasus,
Atlas beetle
Male, Female
http://www.micronet-japan.com/htmls/portfolio/dx_beetle.html
6
Drosophila melanogaster
Male Female
Gynandromorphs
A nearly bilateral gynandromorph of Speyeria diana
(a little extra female on the upper left hindwing),
The left image is the upperside, the right is the underside.
©Irving Finkelstein
Tiger Swallowtail (Papilio glaucus) gynandromorph
(left half male, right half female
©James Adams, 2004
An example of a mosaic individual..
© Marc Perlman, 2004.
Malacosoma disstria gynandromorph (left half male, right half female),
The female abdomen is typically a bit longer than the male, which explains
why the abdomen is curled to the left (the longer female side is on the right).
© James Adams, 2001.
http://www.daltonstate.edu/galeps/Gynandromorphs.htm
7
Triplewart seadevil
Parasitic male
8
Parental investment
(energy and time)
• Two questions:
– How much does each sex invest in offspring?
– Which sex is the limiting resource?
• Parental care is costly
–
–
–
–
No parental care
Maternal care
Paternal care
Bi-parental care
Parental care is costly- no parental care
http://www.edupic.net/lifecycle.htm
9
Parental care is costly- maternal care
Stink bug
http://www.brisbaneinsects.com/brisbane_insects/ParentalCare.htm
Parental care is costly- maternal care
10
Parental care is costly- paternal care
http://magickcanoe.com/blog/2006/07/31/frogs-water-bugs-and-turtles-on-kemptville-creek/
http://www.youtube.com/watch?v=rn-eNYvGCWU
11
Parental care is costly- biparental care
Burying beetles
http://www.youtube.com/watch?v=enazNu0YgPs
Sexual
selection
12
Sexual Selection
“the advantage which certain individuals have
over others of the same sex and species solely
in respect of reproduction”
- The Decent of Man; and Selection in Relation to Sex (1871)
Natural Selection vs.
Sexual Selection
• Natural selection postulates:
– Variation
– Heritable
– Differential reproduction and survival among all individuals of the
population
– Differential reproduction and survival is not random
• Sexual selection:
– All the above but among members of the same sex
13
“There are many other structures and instincts which
must have been developed through sexual selection-such as the weapons of offense and the means of
defense-- of the males for fighting with and driving
away their rivals-- their courage and pugnacity-their various ornaments-- their contrivances for
producing vocal or instrumental music-- and their
glands for emitting odors, most of these latter
structures serving only to allure or excite the female.
It is clear that these characters are the result of sexual and not
of ordinary selection, since unarmed, unornamented, or
unattractive males would succeed equally well in the battle for
life and in leaving a numerous progeny, but for the presence
of better endowed males.”
- The Decent of Man; and Selection in Relation to Sex (1871)
14
Selection pressures for females
• Female reproductive success
– Number of offspring
– Offspring quality
Selection pressures for males
• Male reproductive success
– Number of mates
• Find a mate
• Maintain a mate
– Note: number of mates is a proxy for number of
fertilizations (not necessarily 1:1).
15
Asymmetric selection pressures
• Fundamental asymmetry:
Access to females will be a limiting resource for males, but
access to males will not be a limiting resource for
females.
Bateman’s Principle
1948 Angus John Bateman
Males have evolved an "undiscriminating eagerness"
to mate, whereas females display "discriminating
passivity."
16
Bateman’s data: The number of mates influences the
reproductive success of males more than females
180
males
females
160
Bateman’s gradient
Mean fertility
140
120
100
80
60
40
20
0
0
1
2
3
4
5
Number of mates
Behavioral Consequences of Asymmetric
Selection on Males and Females
• For sex for which access to mates is limited:
– Expect competition
– Intrasexual selection
– Usually males
• For the other sex:
– Expect choosiness
– Intersexual selection
– Usually females
• Investment may be reversed:
– Sex role reversal
http://www.amentsoc.org/insects/glossary/terms/nuptial-gift
17
Intrasexual selection
• Male-male competition
–
–
–
–
–
Combat
Lekking
Territorial defense
Sperm competition
Infanticide (ovicide)
• Alternative reproductive tactics
http://forum.xcitefun.net/animals-sports-play-for-human-entertainment-t43201.html
Combat
http://www.youtube.com/watch?v=ia57rw7PE_8&feature=related
18
Lekking
Lesser wax moth
Achroia grisella
©Ian Kimber
http://mothphotographersgroup.msstate.edu/Files/Live/Species/5000/5623.shtml
Drosophila heteroneura
Drosophila silvestris
19
Hawaiian Drosophila
Territorial/resource defense
http://www.youtube.com/watch?v=vrOFNoicijQ
20
Does mating always lead to
fathering offspring?
• Females mate multiply.
Who fathers the
offspring?
– Sperm competition
– Female cryptic choice
• Do offspring survive to
adulthood?
– Infanticide
How do males compete for
fertilizations within the female?
• Sperm competition (SC)- when the ejaculates of two or more males
overlap in space and time within female reproductive tract
• Adaptations to reduce SC
– Copulatory plugs, mate guarding, extremely large sperm
• Adaptations to increase SC
– Larger ejaculates, more motile sperm
21
Adaptations to reduce SC
• Copulatory plugs
– Spiders, Butterflies
• Mate guarding
– Dung flies
• Sperm removal devices
– Dragonflies
• Chemicals that induce female
refractory period (reduce her
interest in remating)
– Drosophila
• and many more…
Male genitalia damselfly genus Argia.
22
Sperm
Morphology
• Largest sperm relative
to body size:
Drosophila bifurca
(58 mm)
Infanticide (ovicide)
Lethocerus deyrollei
http://en.wikipedia.org/wiki/Lethocerus_deyrollei
23
Alternative Reproductive Tactics (ARTs)
• In some species, if a
male cannot compete
directly, he may
attempt matings
through a different
approach
• Note: not limited to
males, but much
more common in
males
http://www.nature.com/hdy/journal/v82/n3/full/6884930a.html
ARTs: yellow dung flies
• Large males fight over fresh
pats of dung
– Female comes to a pat
– Males compete for her
• Small males look for
females in the grass
• Female lays eggs
immediately after mating,
last male to mate fertilizes
most of the eggs
24
Sneak
ARTs in Dung Beetles
Large male
• Males differ in size and
horns
• Sperm expenditure
differs for the two
morphs
• Residual testis mass of
sneaks is higher than
that of non-sneaks!
Trimorphic dung beetles
α
male
β
male
female
γ
male
25
Intersexual Selection
• What criteria do females use to choose mates?
?
http://www.zandvleitrust.org.za/art-ZIMP%20biotic%20-%20insects%20-%20butterflies.html
Darwin’s dangerous idea:
Female Choice
“Just as man can give beauty, according to his standard of taste, to
his male poultry, or more strictly can modify the beauty originally
acquired by the parent species, can give to the Sebright bantam a
new and elegant plumage, an erect and peculiar carriage-- so it
appears that female birds in a state of nature, have by a long
selection of the more attractive males, added to their beauty or
other attractive qualities. No doubt this implies powers of
discrimination and taste on the part of the female which will at
first appear extremely improbable; but by the facts to be adduced
hereafter, I hope to be able to show that the females actually have
these powers. ”
The Descent of Man, and Selection in Relation to Sex (1871)
26
Female choice (outline)
• Type of choice
• Benefits
– Direct
– Indirect
• Models of indirect choice
Types of female choice
• Cryptic female choice (after mating)
– Sperm ejection
– Sperm re-absorption
– Selective use of sperm
27
http://en.wikipedia.org/wiki/Utetheisa_ornatrix
Selective use of
sperm
Utetheisa ornatrix: female uses sperm from mate she preferred the most.
Largest male sires most offspring
Types of female choice
• Direct choice of mate
28
What do females have to gain by
choosing among males?
Direct benefit- resources, nuptial gifts, etc.
Indirect benefit- genes
Direct benefit: nuptial
gift
29
Balloon flies
http://www.nadsdiptera.org/Doid/Empidchar/Empidchar.htm
www.wikipedia.org
Balloons
•
•
•
•
•
Intact prey
Partially eaten prey
Wrapped prey
Balloons stuck to inedible dried prey
Completely empty balloons
– Balls of silk
– Balls of saliva
30
http://www.youtube.com/watch?v=W1iF3H9xJ-k&feature=related
31
Indirect Benefits:
Models
• Choose a male based on an arbitrary trait that is
“attractive”
– Fisherian runaway selection
• Choose a male based on a high quality trait (indicator) for
genes that improve viability/mating success of offspring
– Sexy-sons hypothesis
– Good genes hypothesis
• Choose a male because he exploits the sensory system
– Sensory bias hypothesis
• Choose a male to avoid exploitation
– Sexually antagonistic coevolution
Fisherian runaway
sexual selection
• Arbitrary
• Experiment:
–
–
–
–
Females are choosy
Male eyestalk length heritable
Female preference heritable
Selection on one trait produces
response in other trait
– Genetic correlation of traits
Stalk eyed flies
32
33
34
Sexy-sons
Spotted cucumber beetles: Diabrotica undecimpunctata howarii
• Females like fast stroking males
– Male strokes females during copulation with their
antennae
• Experiment:
– Females not given choice
• Kids of fast and slow strokers
– Similar numbers/ survival
– Sons resemble dads in stroking rate
» Sons that are fast strokers have more kids
Good genes
• What indicates a male has quality genes?
– Need honest indicator of male quality
– Females use that trait to choose among males
• Zahavi’s Handicap Principle:
– If a male can survive an obvious handicap then he must have superior genes.
– The larger the handicap, the more superior the male must be to survive it, so
females benefit from choosing the most extreme males.
• Honest indicators and good genes
– Female prefers signal
– Only best males can carry signal (true handicap)
– Males with signal leave more/better offspring than males without
35
Drosophila
montana
• Carrier frequency:
– Sensitive to environmental
factors
– Reflects males sexual activity
Hoikkala et al. 1998.
Drosophila montana
Carrier frequency:
– Correlated with offspring
survival
– Female that chooses a male
1 standard deviation from
mean
• 24% increase in viability of
offspring
Hoikkala et al. 1998.
36
Pre-existing sensory bias
• A signal evolves to take advantage of a
sense used for other purposes
• E.g.
– Food preferences
• Many pheromones smell like flowers
– Predator avoidance
Evolution of hearing in Noctuid moths
• Whistling moths signal to females by banging
“castanets” on their wings together.
• Sounds are ultrasonic (approx. 30 kHz).
castanet
37
Evolution of hearing in Noctuid moths
• Most moths cannot hear.
• How did ability to hear ultrasound
evolve in these Noctuid moths?
– Non-hearing Sphingid moths have sensory
cells attached to the cuticle as in Noctuids.
– These supply positional information when
moth vibrates wings.
•
In ancestral Noctuid, sensory cells
could have provided ability to hear
those sounds loud enough to move
cuticle.
What was the likely selection pressure on noctuids
to hear ultrasound?
38
Exploitation of pre-existing biases in
evolution of communication
Noctuids evolved hearing to avoid bats.
Later evolved signaling ability.
Pre-existing
Sensory Bias
Lesser wax moth
Achroia grisella
http://mothphotographersgroup.msstate.edu/Files/Live/Species/5000/5623.shtml
39
Battle of the sexes
• Males and females are in an “arms race”
• As males evolve traits that manipulate females into
mating with them…
…females evolve traits to resist the male manipulation!
• Then males evolve new traits that manipulate females,
which is countered again by the females, etc.
Antagonistic
Sexual
Coevolution
•
•
•
•
Female: mate as many times as possible with best males
Male: female should only mate with him
More coercion and resistance
E.g. Drosophila
– male seminal fluid influences female behavior
• delay remating with another male.
– Females have evolved resistance to effects of males
40
Antagonistic sexual
selection between male
and female fruit flies
Sex role reversal
• Usually females invest more in offspring than
males.
– Females are then more choosy
• Sometimes the roles are reversed
– When reversed (males make more of an investment),
then males are more choosy
41
An Australian katydid
• Males call to attract
females.
• Male produce a
spermatophylax.
• Females prefer males
with little silence
between calls.
http://www.flickr.com/search/groups/?q=katydid&w=642290%40N21&m=pool
Sexual SelectionAustralian katydid
• Females produce several hundred eggs.
• Males produce millions of sperm
– In good conditions, males may produce more than one spermatophylax
• Spermatophylax:
– Gooey masses of protein that the female eats to nourish her eggs
– Up to 25% of the weight of the male
• Females produce more successful eggs with a big spermatophylax
• A male that can produce more than one can mate more than once
– Big males produce a big spermatophylax
– Big males sing more
• Thus, males with the fastest singing rate attract the most
females. Females are picky and choose big males.
42
Sexual Selection ReversedAustralian katydids
Mormon cricket
http://people.uleth.ca/~dan.johnson/fieldtrips.htm
• In bad conditions (low food), few males can make more than
one spermatophylax.
• Males are then limited in the number of times they can mate
– Males become picky.
• Females compete for males and not all females mate.
– Large females are more successful than small females.
Variation in courtship behavior:
fruit flies (Drosophila species)
• Closely related species
– Behave differently and/or
– Have different courtship songs
• May be:
– Selection for species mate recognition
– Sexual selection
43
D. melanogaster courtship
Greenspan 1995
D. nebulosa courtship
44
D. nebulosa courtship
45
Amplitude
D. sturtevanti
Time (seconds)
Amplitude
D. emarginata
Time (seconds)
46
Complicated patterns of song evolution in D. saltans group
austrosaltans
Low amplitude secondary
Doublet primary song
prosaltans
saltans
Loss of one song
lusaltans
Modification to rasps
emarginata
neocordata
Two songs
dacunhai
Doublet primary song
milleri
Beeps
sturtevanti
subsaltans
willistoni
Number of songs
Changes to primary
Changes to secondary
Phylogeny: Mort et al. in prep.
Songs: Gleason et al. in prep.
Suggested Reading
2003 Holt Paperbacks
47
Suggested Readings
•
Technical press:
– Andersson, Malte (1994) Sexual selection. Princeton University Press.
– Arnquist, Goren and Locke Rowe (2005). Sexual Conflict. Princeton University
Press.
– Darwin, Charles. (1871). The Descent of Man and Selection in Relation to Sex.
John Murray.
– Eberhard, William (1996) Female Control: Sexual Selection by Cryptic Female
Choice. Princeton University Press.
– Olivera, Rui, F., Michael Taborsky, and H. Jane Brockman, editors. (2008).
Alternative Reproductive Tactics: An Integrative Approach. Cambridge University
Press.
– Searcy, William A. (2005) The Evolution of Animal Communication: Reliability
and Deception in Signaling Systems. Princeton University Press.
– Shuster, Stephen, M. (2003). Mating Systems and Strategies. 2008. Princeton
University Press.
Suggested Readings
•
Popular Press
– Miller, Geoffrey. (2001). The Mating Mind: How Sexual Choice Shaped the
Evolution of Human Nature. Anchor.
– Ridley, Matt. (2003). The Red Queen: Sex and the Evolution of Human Nature.
Harper Perennial
48