Upload
others
View
10
Download
0
Embed Size (px)
Citation preview
1
Sex Role Reversal and Sexual Selection in Seahorses and Pipefish
Stephen M. ShusterNorthern Arizona University
Sex Role Reversal•Males provide parental care.•Females seek multiple mates.
•Sexual dimorphism is
reversed.
2
Extreme Cases are Important for Understanding Sexual Selection
The sex-difference in the Variance in Relative Fitness is reversed,
VWfemales >> VWmales.
Female Male
3
Syngnathid Fish•Are among the
best known of sex role reversed
species.•Variable in degree
of reversal.•Phylogeny is well
understood.
The Goal:To use the degree of sex-role reversal in
Syngnathid fishes to compare Parental Investment Theory
with The Opportunity for Selection
as measures of the sex-difference in the intensity of sexual selection.
Syngnathid Genera of Interest
4
Nerophis(Strongly Role Reversed)
Males brood embryos externally.
Females initiate courtship.
Males are choosy; females are not.
Females inhibit the courtship displays of smaller females.
Females much larger than males, with blue skin folds.
Syngnathus(Moderately Role Reversed)Male brood pouch with sealed folds.
Both sexes active in courtship; females faster than males.
Both sexes choosy about size; M>F.
Females inhibit egg production in smaller females.
Females slightly larger than males, show pigment displays during courtship.
Hippocampus(Conventional Sex Roles)
Male brood pouch internal.
Males compete more to become pregnant than females compete to mate.
Both sexes are choosy about size.
Pairs are faithful; male aggression observed, but rarely.
Sexes are monomorphic.
5
SyngnathidPhylogeny
Conventional sex roles are NOT
ancestral.Mating system
evolution is NOT constrained by
phylogeny.
Two Theoretical Frameworks
Parental Investment Theory(PIT)
Bateman 1948; Williams 1966; Trivers 1972; Emlen & Oring 1977; Maynard Smith 1977; Clutton-Brock & Vincent 1991; Clutton-Brock &
Parker 1992; Ahnesjö et al. 2001.
The Opportunity for Selection(OS)
Crow 1958, 1962; Wade 1979; Wade & Arnold 1980; Arnold &Wade 1983; Wade 1995; Shuster & Wade 1991, 2003.
Parental Investment Theory•The sex difference in initial parental investment causes sexual selection.•Generates three
predictions for sex role reversed
species.
6
Predictions of PIT for Syngnathids
1. Male Investment > Female Investment
{Male – Female} Investment
Nerophis > Syngnathus > Hippocampus
Predictions of PIT for Syngnathids
2. Operational Sex Ratio = Strength of Sexual Selection
OSR (= Nfemales/Nmales)
Nerophis > Syngnathus > Hippocampus
Predictions of PIT for Syngnathids
3. Male Availability Limits Female Reproduction: A Sex-Difference in
Potential Reproductive Rate“The maximum number of independent offspring that
parents can produce per unit time (p. 60; Clutton-Brock & Vincent 1991).”
{Female – Male} PPR
7
Measuring PRR
•Allow members of each sex unlimited
opportunities to mate in controlled setting.
•PRR=Xoffspring/unit time.
Predictions of PIT for Syngnathids
3. A Sex-Difference in Potential Reproductive Rate
{Female – Male} PPR
Nerophis > Syngnathus > Hippocampus
Data: A Sex Difference in Initial Parental Investment
Nerophis1. Males suffer greater predation risk (Svennson 1988)
2. Males invest less in gametes than females (Berglund et al. 1986; 1989)
Syngnathus1. Males feed less than females (Svensson 1986).
2. Male and female investment in gametes is about equal (Berglund et al. 1986; 1989).
Hippocampus1. Females have higher energy expenditure than males
(Masonjones & Lewis 2000).
8
1. Male Investment > Female Investment{Male – Female} Investment
Prediction:++Nerophis > +Syngnathus > 0 Hippocampus
Observation:0 Syngnathus > - Nerophis > - - Hippocampus
PIT Prediction vs Observation
Data: The Operational Sex Ratio (OSR)
Nerophis1. Equal in nature (Berglund et al. 1989).
Syngnathus1. Equal in nature (Berglund et al. 1989).
2. Variable, but usually female biased (Vincent et al. 1993).3. Consistently female biased (Berglund & Rosenqvist 1993; Jones et al. 1999).
Hippocampus1. Not biased in mated males, male biased with unmated males
(Vincent 1994; Vincent and Sadler 1995).
2. Operational Sex Ratio = Strength of Sexual Selection, OSR (= Nfemales/Nmales)
Prediction:1++Nerophis > 1+ Syngnathus > 1 Hippocampus
Observation:1+? Syngnathus > 1 Nerophis > -1? Hippocampus
PIT Prediction vs Observation
9
Data: A Sex Difference in PRRNerophis
1. Much greater for females, males mate once per cycle, females mate >1 (Berglund et al. 1989; McCoy et al. 2001).
Syngnathus1. Females produce more eggs than males can care for
(Berglund et al. 1988; 1989; 2.7X, Berglund & Rosenqvist; Jones et al. 2000).
Hippocampus1. Identical under natural conditions
(Vincent 1994; Vincent and Sadler 1995).
2. 17% greater for males under laboratory conditions (Masonjones & Lewis 2000).
3. Male Availability Limits Female Reproduction: A Sex-Difference in
Potential Reproductive Rate{Female – Male} PRR
Prediction:Nerophis > Syngnathus > Hippocampus
Observation:++Nerophis = ++Syngnathus > Hippocampus
PIT Prediction vs Observation
Summary: PIT #1
• Observed Sex-Difference in
GameticInvestment not
in predicted order.
•Syngnathus has female investment equal to males.•Nerophis females invest more than males.
•Hippocampus females invest much more than males.
10
Summary: PIT #2
• Observed OSRs not
in predicted
order.
•Most sex-reversed, Nerophis, does not have predicted excess of females.
•Unexpected female excess observed in Syngnathus.•Expected male excess in Hippocampus…?
Summary: PIT #3• Observed Sex-Difference in
PRR consistent with predictions but not
consistent with observed dimorphism in Nerophis and
Syngnathus.
•Also, estimates of PRR require study-specific manipulation and
lack confidence limits.
The Opportunity for Selection•The sex difference in the
variance in mate numbers causes sexual selection.
•Provides a direct measure of the intensity of sexual selection.
•Allows phylogenetic comparisons and calculation of
confidence limits.•Provides an empirical estimate of the degree to which the sexes
will diverge.
11
What Is Measured?
I = VW/W2
•Compares the fitness of breeding parents relative to the pre-reproductive
population.•The variance in offspring numbers for
each sex is divided by the squared average in offspring numbers.
Ifemales - Imales = Imateswhen R = 1.
The Sex Difference in the Opportunity for Selection
Ifemales - Imales = (R-1) (Imales) + Imateswhen R ≠ 1.
The Opportunity for Selection
•In sex role reversed species,
VWfemales >> VWmales
•This relationship generates three
predictions.
12
Predictions of OS for Syngnathids
1. A Sex-Difference in the Variance in Offspring numbers
{VOfemales – VOmales}
Nerophis > Syngnathus > Hippocampus
Predictions of OS for Syngnathids
2. A Sex-Difference in the Opportunity for Selection
{Ifemales – Imales}
Nerophis > Syngnathus > Hippocampus
Predictions of OS for Syngnathids
3. Imates is Large Relative to Ifemales
{Imates / Ifemales}
Nerophis > Syngnathus > Hippocampus
13
We Need to Measure:
The variance in offspring numbers for females and for males.
Prediction 1. A Sex-Difference in the Variance in Offspring Numbers
{VOfemales – VOmales}
The Mean and Variance in Offspring Numbers
NOtotal = 25
O♀♀= 5; VO♀♀= 0; N=5.
O♂♂=5; VO♂♂= 0; N=5.
NOtotal = 25
O♀♀= 5; VO♀♀= 0; N=5.
O♂♂=5; VO♂♂= 0; N=5.
The Mean and Variance in Offspring
Numbers, by Sex
14
NOtotal = 25
O♀♀= 5; VO♀♀= 10; N=5.
O♂♂=5; VO♂♂= 0; N=5.
If One Female Mates Twice...
NOtotal = 25
O♀♀= 5; VO♀♀= 20; N=5.
O♂♂=5; VO♂♂= 0; N=5.
If One Female Mates Five
Times...
NOtotal = 25
O♀♀= 5; VO♀♀= 0; N=5.
O♂♂=5; VO♂♂= 20; N=5.
If One Male Mates Five
Times...
15
When some individuals are excluded from mating, the
variance in offspring numbers is increased.
This is the source of sexual selection.
Nerophis ophidion(Berglund et al. 1989)
Measured PRR using 15 females, 27 males
O♂♂=204±82, N=27; VO♂♂=6,724
H♀♀=1.8±0.7, N=15
If R = 1 as in nature,
then pS♀=15/27 = .555
And p0♀ = 1 - pS♀ = .445
The Distribution of Males with Females
pi♀ i i pi♀___________________________________________________________
p0♀ =12/27=.445 0 0
p1♀ = 5/27=.185 1 .185
p2♀ = 8/27=.296 2 .592
p3♀ = 2/27=.074 3 .222
∑ 1.000 1.000
Σ i pi♀ = M♀♀
16
VO♀♀total = VO♀♀within + VO♀♀among
= The average of the variances in offspring number within the classes of mating females
+The variance of the averages in offspring number
among the classes of mating females
The Total Variance in Female Offspring Number
VO♀♀within = Σ pi (iVO♂♂)
= (.445)[(0)(6,724)] + (.185)[(1)(6,724)] + (.296)[(2)(6,724)] + (.074)[(3)(6,724)]
= 0 + 1,234.9 + 3,980.6 + 1,492.7
= 6,717.3
The Variance in Offspring Number Within Females
VO♀♀among = Σ pi (MO♂♂-iO♂♂)2
= (.445)[204-(0)204]2 + (.185)[204-(1)204]2
+ (.296)[204-(2)204]2 + (.074)[204-(3)204]2
= 18,519.1 + 0 + 12,318.3 + 12,318.3
= 43,155.8
The Variance in Offspring Number Among Females
17
VO♀♀total = VO♀♀within + VO♀♀among
= 49,873.1And,
VOfemales – VOmales
= 49,873.1 - 6,724
= 43,149.1
The Sex Difference in the Variance in Offspring Numbers
1. A Sex-Difference in the Variance in Offspring numbers {VOfemales – VOmales}
Prediction:Nerophis > Syngnathus > Hippocampus
Observation:
Nerophis > Syngnathus > Hippocampus
43,149.1 > 6,275.3 > -18.7(Berglund et al. 1989; Vincent & Sadler 1995)
OS Prediction vs Observation
We Need to Measure:
The opportunity for selection on females and on males.
Prediction 2. A Sex-Difference in the Opportunity for Selection
{Ifemales – Imales}
18
Syngnathus typhle(Berglund et al. 1989)
Measured PRR using 25 females and 43 males
∑ i pi♂=P*♂♂= 3.33±0.64 matings/maleO♀♀/mating=23; VO♀♀/mating=324,
N=43
0
5
10
15
20
25
30
35
0 1 2 3 4 5 6
N Matings
N M
ales
VO♂♂total = VO♂♂within + VO♂♂among
= The average of the variances in offspring number within the classes of mating males
+The variance of the averages in offspring number
among the classes of mating males
The Total Variance in Male Offspring Numbers
VO♂♂within = Σ pi (iVO♀♀/mating)
= (.023)[(2)(324)] + (.698)[(3)(324)] + (.209)[(4)(324)] + (.070)[(5)(324)]
= 15.1 + 678.1 + 271.3 + 113.0
= 1,077.5
The Variance in Offspring Number Within Males
19
VO♂♂among = Σ pi (O♂♂ - iO♀♀/mating)2
= (.023)[77-(2)(23)]2 + (.698)[77-(3)(23)]2
+ (.209)[77-(4)(23)]2 + (.070)[77-(5)(23)]2
= 21.8 + 40.2 + 49.7 + 102.9
= 214.6
The Variance in Offspring Number Among Males
VO♂♂total = VO♂♂within + VO♂♂among
= 1,292.1 And,
Imales = VO ♂♂ / O♂♂2
= 1,292.1 / (76.6)2
= 0.22
The Opportunity for Selection on Males
Syngnathus typhle(Berglund et al. 1989)
Measured PRR using 25 females and 43 males,But R = 1 in nature.
∑ i pi♀=P♀♀= 1 mate/female (=3.33 matings/mate)
O♂♂=76.6, VO♂♂=1,292.4, N=43
0
5
10
15
20
0 0.5 1 1.5 2 2.5 3 3.5 4
N Filled Males
N F
emal
es
20
VO♀♀total = VO♀♀within + VO♀♀among
= The average of the variances in offspring number within the classes of mating females
+The variance of the averages in offspring number
among the classes of mating females
The Total Variance in Female Offspring Numbers
VO♀♀within = Σ pi (iVO♂♂ ) = (.442)[(0)(1,292)] + (.023)[(.5)(1,292)] + (.093)[(1)(1,292)] + (.209)[(1.5)(1,292)]+ (.070)[(2)(1,292)] + (.116)[(2.5)(1,292)]+ (.023)[(3)(1,292)] + (.023)[(3.5)(1,292)]
= 0 + 15.0 + 120.2 + 405.7 + 180.3+ 375.6 + 90.1 + 150.2
= 1,292.1
The Variance in Offspring Number Within Females
VO♀♀among = Σ pi (MO♂♂-iO♂♂)2
= (.442)[77-(0)(77)]2 + (.023)[77-(.5)(77)]2
+ (.093)[77-(1)(77)]2 + (.209)[77-(1.5)(77)]2
+ (.070)[77-(2)(77)]2 + (.116)[77-(2.5)(77)]2
+ (.023)[77-(3)(77)]2 + (.023)[77-(3.5)(77)]2
= 2,592.0 + 34.1 + 0 + 306.9 + 409.3+ 1,534.7 + 545.7 + 852.6
= 6,275.3
The Variance in Offspring Number Among Females
21
VO♀♀total = VO♀♀within + VO♀♀among
= 7,567.4 And,
Ifemales = VO♀♀ / O2♀♀
= 7,567.4 / (76.6)2
= 1.29
The Opportunity for Selection on Females
Ifemales - Imales = Imateswhen R = 1.
The Sex Difference in the Opportunity for Selection
In Syngnathus,
1.29 – 0.22 = 1.07
2. A Sex-Difference in Opportunity for Selection {Ifemales – Imales}
Prediction:
Nerophis > Syngnathus > HippocampusObservation:
Syngnathus > Nerophis > Hippocampus
{1.29-.22}=1.07 > {1.20-.16}= 1.04 > {.64-.65}= -.01(Berglund et al. 1989; Vincent & Sadler 1995)
OS Prediction vs Observation
22
Nerophis ophidion(Berglund et al. 1989)
0
5
10
15
20
25
30
0 1 2 3
N Mates
N M
ales
0
2
4
6
8
10
12
14
0 1 2 3 4
N Mates
N F
emal
es
Only females have multiple mates; with sexual selection,
sexual dimorphism is pronounced.
Syngnathus typhle(Berglund et al. 1989)
0
5
10
15
20
0 0.5 1 1.5 2 2.5 3 3.5 4
N Filled Males
N F
emal
es
0
5
10
15
20
25
30
35
0 1 2 3 4 5 6
N Matings
N M
ales
Males and females have multiple mates; with sexual selection on both sexes, sexual dimorphism
is reduced.
We Need to Measure:
The sex difference in the opportunity for selection on females
and on males.
Prediction 3. Imates is Large Relative to Ifemales
{Imates / Ifemales}
23
Hippocampus fuscus(Vincent and Sadler 1995)
51 females, 47 males in nature
∑ i pi♂=P*♂♂=P♂♂= 0.89±0.52matings/male
O♀♀/mating=40.2; VO♀♀/mating=670.8, N=42
0
10
20
30
40
0 1 2 3
N Mates
N M
ales
VO♂♂total = VO♂♂within + VO♂♂among
= The average of the variances in offspring number within the classes of mating males
+The variance of the averages in offspring number
among the classes of mating males
The Total Variance in Male Offspring Numbers
VO♂♂within = Σ pi (iVO♀♀/mating)
= (.191)[(0)(671)] + (.723)[(1)(671)] + (.085)[(2)(671)]
= 0 + 485.3 + 114.2
= 599.4
The Variance in Offspring Number Within Males
24
VO♂♂among = Σ pi (O♂♂ - iO♀♀/mating)2
= (.191)[40-(0)(40)]2 + (.723)[40 -(1)(40)]2
+ (.085)[40 -(2)(40)]2
= 309.5 + 0 + 137.5
= 447.0
The Variance in Offspring Number Among Males
VO♂♂total = VO♂♂within + VO♂♂among
= 1,046.4 And,
Imales = VO ♂♂ / O♂♂2
= 1,046.4 / (40.2)2
= 0.65
The Opportunity for Selection on Males
Hippocampus fuscus(Vincent and Sadler 1995)
∑ i pi♀= P*♀♀= P♀♀= 0.82±0.51 matings/female
O♂♂/mating=40.2; VO♂♂/mating=270.8, N=42
0
10
20
30
40
0 1 2 3
N Mates
N F
emal
es
25
VO♀♀total = VO♀♀within + VO♀♀among
= The average of the variances in offspring number within the classes of mating females
+The variance of the averages in offspring number
among the classes of mating females
The Total Variance in Female Offspring Numbers
VO♀♀within = Σ pi (iVO♂♂ )
= (.235)[(0)(671)] + (.706)[(1)(671)] + (.059)[(2)(671)]
= 0 + 473.5 + 78.9
= 552.4
The Variance in Offspring Number Within Females
VO♀♀among = Σ pi (MO♂♂-iO♂♂)2
= (.235)[40-(0)(40)]2 + (.706)[40 -(1)(40)]2
+ (.059)[40 -(2)(40)]2
= 380.2 + 0 + 95.1
= 475.3
The Variance in Offspring Number Among Females
26
VO♀♀total = VO♀♀within + VO♀♀among
= 1,027.7 And,
Ifemales = VO♀♀ / O2♀♀
= 1,027.7 / (40.2)2
= 0.64
The Opportunity for Selection on Females
Ifemales - Imales = Imateswhen R = 1.
The Sex Difference in the Opportunity for Selection
In Hippocampus,
0.64 – 0.65 = -0.01
RHfuscus = 51♀♀/47♂♂ = 1.085
However, R > 1
Thus,Ifemales - Imales = (R-1) (Imales) + Imates
AndImates(adj) = 0.067
27
That is, how much of selection on males is due to
sexual selection?
Imates / Ifemales = 0.067 / 0.636
= 0.103
How Much of Ifemales is Imates?
3. Imates is Large Relative to Ifemales {Imates / Ifemales}
Prediction:
Nerophis > Syngnathus > HippocampusObservation:
Nerophis > Syngnathus > Hippocampus
.87 > .84 > .10(Berglund et al. 1989; Vincent & Sadler 1995)
OS Prediction vs Observation
Summary: OS #1
• Observed Sex-Difference in Variance in
Offspring number consistent with
predictions.
•Relative magnitudes of {VOfemales – VOmales} are consistent with observed sexual dimorphism in all
genera.
28
Summary: OS #2
• Observed {Ifemales-Imales}
not in predicted order.
•BUT, magnitude of Imales is smaller in Nerophis than in Synganthus, in which females and males seek multiple
mates.
Summary: OS #3
• Observed Imates/Ifemalesconsistent with
predictions.
•Relative magnitudes of Imates/Ifemales consistent with observed sexual
dimorphism in all genera.
Conclusion I: OS = PIT?•NO!
•The OS method provides a direct
measure of selection intensity.
•The PIT approach relies on proxies for selection intensity.
29
Conclusion I: OS = PIT?•The sex difference in the opportunity for selection
is both necessary and sufficient to account for
differences in sexual dimorphism.
•The correlation between sex differences in gametic/parental
investment and sexual dimorphism is poor.
Conclusion II: OS > PITFor measuring the intensity of sexual selection within and among populations,the Opportunity for
Selection approach is:More quantitative.Easily interpreted.
Evolutionarily meaningful.
Sexual Selection:Its Not Just for
Males Anymore.