Sexual Selection and Mating Systems
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1 Sexual Selection and Mating Systems In the Light of Evolution III: Two Centuries of Darwin Arthur M. Sackler Colloquia of the National Academy of Sciences Stephen M. Shuster Northern Arizona University
2 Outline.Darwin s contributions 2.Existing emphases in plant and animal mating systems 3.Quantitative approaches 4.Combining and improving methodologies 5.Conclusions
3 Sexual Dimorphism and Sexual Differences: The Chillingham Bull, by Thomas Bewick
4 Darwin s s Observations On Sexual Differences Focused mainly on the contexts in which sexual selection occurred Male-male combat Female mate preferences An emphasis that persists to this day.
5 Sexual Selection " depends, not on a struggle for existence, but on a struggle between males for possession of the females; the result is not death of the unsuccessful competitor, but few or no offspring. Sexual selection is, therefore, less rigorous than natural selection (859, p. 88).
6 Is There A Conflict? How can sexual selection appear to be one of the most powerful evolutionary forces known, Yet Darwin himself considered sexual selection less rigorous than natural selection?
7 The Cause of Sexual Selection If each male secures two or more females, many males would not be able to pair (Darwin 87, p. 266).
8 Visualizing the Process Wade 979; Shuster and Wade 23 When each male mates once, all males are equally successful. When some males mate more than once, other males are excluded from mating at all. Number of males Number of males Mates per male Mates per male
9 Sexual Selection Creates Two Classes of Males If p S equals the fraction of males in the population who mate, and p (= p S ) equals the fraction of males that do not mate, Number of males H Mates per male H = N females / ( p )
10 Graphically, p = -(/ (/H) Shuster & Wade 23; Wade & Shuster 24 Proportion of nonmating males (p) Harem Size (H)
11 Sexual Selection is a Powerful Evolutionary Force Because: For every male who sires young with with k females, there must be k- males who fail to reproduce at all. Shuster & Wade 23
12 Darwin on Animal Mating Systems Sexual Selection is NOT Ubiquitous in Animals In many cases, special circumstances tend to make the struggle between males particularly severe. (Darwin 87, p. 28).
13 Darwin s s Grasp of Animal Mating Systems The special circumstances in which reproduction occurs within individual species. It is here that sexual differences arise - or do not.
14 Darwin on Plant Mating Systems Selfing is NOT Ubiquitous in Plants Various hermaphrodite plants have become heterostyled, and now exist under two or three forms; and we may confidently believe that this has been effected in order that crossfertilisation should be assured. (Darwin 877, p. 266).
15 Darwin s s Grasp of Plant Mating Systems Certain physical structures of flowers prevent or allow selfing. It is here that floral differences arise - or do not.
16 Since Darwin Two Descriptions of Mating Systems: In terms of the genetic relationships that exist between mating male and female elements (Plants) In terms of the numbers of mates per male or per female (Animals)
17 Plant Mating Systems Darwin 877; Wright 922; Fisher 94; Clegg 98; Lande & Schemske 985; Holsinger 99; Barrett and Harder 996; Vogel and Kalisz 22 A focus on deviations from random mating and their associated genetic consequences. Differences in mating system identified in terms of floral morphology.
18 A Summary of Plant Mating Systems Perfect Flowers (hermaphroditic) Imperfect Flowers Selfing Self-pollination Cross-pollination Heterostyly Physical separation of style and stamen Dichogamy Temporal separation of anter / stigma maturation. Self Incompatibility Monoecy Dioecy Outcrossing Autogamy, cleistogamy Chasmomogamy Distyly, tristyly Protandry, protogyny Sporophytic, gametophytic Androdioecy/monoecy Gynodioecy/monoecy After R. Cronn
19 Sexual Selection in Plants? Willson & Burley 983; Cruzan 988; 993; Slogsmyr & Lankinen 22; Shuster & Wade 23 Male plants can compete with one another through pollen production and pollen tube growth on the female stigmatic surface in a manner analogous to sperm competition between males within multiply inseminated females in insects. However, this kind of male-male competition through pollen does not necessarily result in greater variance in male than in female reproductive success.
20 Animal Mating Systems (Bateman 948; Williams 966; Trivers 972; Emlen & Oring 977; Maynard Smith 977; Clutton-Brock & Vincent 99; Clutton-Brock & Parker 992; Reynolds 996; Ahnesjö et al. 2; Alcock 25) Parental Investment Theory: Gamete dimorphism initiates sexual selection. The few, large ova of females are a limited resource for which males must compete. The intensity of sexual selection on males depends on the degree to which females are rare.
21 The Environmental Potential for Polygamy (EPP) Emlen & Oring 977 The degree to which the social and ecological environment allows males to monopolize females as mates. However, EPP is difficult to define and quantify among species.
22 The Operational Sex Ratio Emlen & Oring 977 OSR = N mature males /N receptive females A reproductive competition coefficient. OSR> = females are rare, competition for mates is intense. OSR< = females are abundant, competition for mates is relaxed.
23 Evolutionary Interpretations Biases in OSR are presumed to have significant consequences Variance in mating success: (Positive effect: Emlen 976; Balshine-Earn 996; Kvarnemo et al. 995; Jann et al. 2; Jones et al. 2; Foellmer & Fairbairn 25; Negative effect: Shuster et al. 2; No effect: Cerchio et al. 25; Reversal of sex roles: (Emlen & Oring 977; Smith 984; Berglund et al. 989; Forsgren et al. 24; Andersson 25; Simmons & Kvarnemo 26) Avoidance of sperm competition (Positive: Møller 989; Møller & Briskie 995; Hosken 997; Bateman 997; Pitnick & Karr 996; Negative: Pen & Weissing 999; Kemp & Macedonia 27) Mate selection and choosiness: (Rosenqvist 993; Berglund 994; Kokko & Monahagn 2) Mate guarding/mating duration (McLain 98; Sillen-Tullberg 98; Jormalainen 998; Gao & Kang 25) Family sex ratio adjustment McLain & Marsh 99; Lopez & Dominguez 23; Warner & Shine 27; Aggressive behavior Grant et al. 2; Grant & Foam 22; Changes in oviposition rate Spence & Smith 25; Female body temperature: (Alsop et al. 26) Population declines: (Stifetten & Dale 26)
24 Measuring OSR (Clutton-Brock & Vincent 99; Clutton-Brock & Parker 992; Parker & Simmons 996; Ahnesjö et al. 2; Forsgren et al. 24) Considers the effect of certain receptive individuals at a particular time and in a particular place, on the intensity of sexual selection.
25 Problems with Leaving Certain The justification for this is that only certain individuals reproduce at any time; Including everyone could bias estimates of competition intensity. Specifically, leaving individuals out causes errors in estimates of actual selection. Individuals Out
26 N Males N Males m =. V m = Mates per male m =.56 V m = Mates per male When Losers are Ignored A significant fraction of the among-group group component of fitness variance goes unrecognized. This creates 2 kinds of errors:. The average fitness of the population is overestimated 2. The variance in fitness for the population is underestimated
27 And, the Stronger Sexual Selection Becomes, Proportion of nonmating males (p) Harem Size (H) The larger the possible error! Because as fewer males mate, more of the male population is excluded from mating altogether.
28 A Better Approach Measure Selection Directly If traits under selection are known, Measure the standardized covariance between phenotype and fitness slope of this line is β. Bateman gradients Jones, Arguello & Arnold 22 Proc. Roy. Soc. Lond. B: Biol. Sci.
29 Phenotypic Correlations What happens when particular individuals in a population mate with other particular individuals? When particular traits become associated between the sexes, genetic correlations may arise between male and female After Bakker 993 mating phenotypes.
30 Genetic Correlations Genetic Fisher 93; Lande 98; Kirkpatrick 982; Bakker 993 Relative fitness.5 Bright males Choosy females Nonchoosy females Dull males
31 Other Genetic Correlations Shuster & Wade 23 Relative fitness.5 Solitary females Grouped females Nonaffilative Nonaffiliative males Affiliative males
32 What If You Can t Measure Selection On Specific Traits?
33 The Opportunity for Selection (Crow 958, 962; Wade 979) I = V W /W 2 = V w Compares the fitness of breeding parents relative to the population before selection. The variance in relative fitness, V w, provides an empirical estimate for selection s strength. I = V O /(O ) 2 I = V O /(O ) 2
34 The Sex Difference in the Strength of Selection, I Shuster & Wade 23 I I = { I - I } = I mates When I >, sexual selection modifies males When I <, sexual selection modifies females When I =, either there is no sexual selection Or sexual selection is equally strong in both sexes
35 Parental Investment and Animal Mating Systems (Bateman 948; Williams 966; Trivers 972; Emlen & Oring 977; Maynard Smith 977; Clutton-Brock & Vincent 99; Clutton-Brock & Parker 992; Reynolds 996; Ahnesjö et al. 2; Alcock 25) Males and females are defined by differences in energetic investment in gametes. In most sexual species, females produce few, large ova, whereas males produce many, tiny sperm.
36 However, Sex differences in parental investment fail to explain the details of male parental care. In sticklebacks, male care enhances a male's ability to mate. In seahorses, male care reduces male mating opportunities. How is this possible if parental investment is causal?
37 Hippocampus I = [I - I ] =. I / I =. Syngnathus I = [I - I ] = -.88 I / I = 5.4 Vincent & Sadler 994 Berglund et al. 989 Gasterosteus I = [I - I ] = 2.3 I / I = 6. Goldschmidt et al. 993 Nerophis I = [I - I ] = -.4 I / I = 7.4 Berglund et al. 989
38 What If You Can t Quantify Offspring Numbers in Males and Females?
39 Sexual Selection and the Spatio- Temporal Distribution of Matings c.f. Shuster & Wade 23 Does OSR reliably estimate the intensity of competition? Consider: Equal sex ratio (5 males: 5 females). 5 male territories, 5 females with variable receptivity
40 Possible Measurements: N.j = N females in each interval N i. = N females in each row K(t) = N males in all territories R = N females /N males R O = N males /N females = OSR R (t) = N i. /K(t) = R at each interval R O (t) = K(t)/N i. = R O at each interval Σ R O (t) = the sum of the individual instantaneous OSRs Σ R (t) = the sum of the individual instantaneous Rs
41 Patches w/ males K(t) R(t) Ro(t) /N females (t) Scenario : Intervals w/ females-> Σ 5 N.j N i. 5
42 Scenario 2: Intervals w/ females-> Patches w/ males Σ N.j 5 K(t) R(t) Ro(t) /N females (t) N i.
43 Scenario But there is a Problem Scenario 3: 2 Intervals w/ females-> Patches w/ males Σ N.j 5 K(t) R(t) Ro(t) /N females (t) N i. Scenarios and 2 are clearly distinct in the number of males that mate. Yet their instantaneous OSRs [R O (t)] are identical! Also, while ΣR(t)=R=R O =, ΣR O (t) = 25. Each R O (t) overestimates the overall effect of competition among males.
44 A Solution: Partitioning Variance Components V total = V within + V among = The average of the variances within the classes (groups) + The variance of the averages among the classes (groups)
45 Intervals w/ females-> Patches w/males Σ 5 N.j 5 K(t) (R t ) Ro(t) Vti I mates (t) (R(t)/R) *I mates (t) N i. V Nij V Nij N i. /T V(k) I mates (k) A Solution! Shuster & Wade 23 pp. 94- Nij N females = V mates(t /N males (t) + V = (R[t R I mates Nij = V t(k (k) + (V mates mates = V mates (R[t]) mates )/(T) 2 mates /R 2 I mates I mates V mates mates = (T)( (T/R( T/R) 2 {V (R[t]) + (V mates(t) - V mates = I sex ratio + (* Imates(t t(k t(k (k) (k) )} )} (t) - * I mates mates(k) )
46 What Does It Mean? Imates= I s + ( * I - * I ex ratio mates(t (t) mates mates(k)) The total opportunity for sexual selection The opportunity for sexual selection caused by temporal variation in the sex ratio (a better OSR ) The opportunity for sexual selection caused by temporal variation in the availability of females minus The opportunity for sexual selection caused by spatial variation in the availability of females
47 What If You Can t Quantify Mating Success?
48 The Mean Crowding of Females in Space and Time Lloyd 967; Wade 995; Shuster & Wade 23 The mean crowding of females on resources defended by males can be expressed as, m* = m + [(V m / m) -] In this context, m* represents the number of other females the average female experiences on her resource patch. t* = t + [(V t / t)-]
49 Spatial Distribution of Mates m* = m + [(V m / m) m - ] m* = large m* = small a b Shuster & Wade 23
50 Temporal Distribution of Mates t* = t + [(V t / t) t - ] a t* = large t* = small Time b Time Shuster & Wade 23
51 m*, t* and I mates mates (= (= I) The relationship between m* and I mates is proportional. At m* max one or a few males could defend and mate with all of the females in the population. Conversely, the relationship of between t* and I mates is reciprocal. At t* max, the ability of one or a few males to mate with multiple females is reduced. 2 Imates Imates 2 2 m* 2 a b t*
52 The I Surface I m* t*.5. Shuster & Wade 23
53 Dynamic Evolution of Mating Systems When m* is low and t* is high: Males are likely to seek out, remain with, and provide parental care for isolated, synchronously receptive females Persistent Pairs Shuster & Wade 23
54
55 If Females Become More Spatially Aggregated: m* is moderate to high, t* is high: Males are expected to defend individual females, but breeding will occur in large aggregations. Mass Mating
56
57 Polygamy Occurs When The mean spatial crowding of matings, m*, and the mean temporal crowding of matings, t* are both moderate.
58
59
60 If Male Traits Attract the Attention of Females Then m* increases and the t* decreases. And sexual selection can become intense
61
62 The I Surface I m* t*.5. Shuster & Wade 23
63 The Ecology and Phenology of Plant Mating Systems outcrossers dioecy wind pollinated dichogamy heterostyly animal pollinated selfers H M L Spatial crowding m* H M L Temporal crowding t*
64 How are Plant and Animal Mating Systems Related? The effects of m* and t* may be more moderate in plants than in animals.
65 Summary Why not to use the same quantitative methods for studying plant and animal mating systems? Population genetics rigor and emphasis on genetic parentage data from plants. Spatio-temporal data and quantitative genetic approaches to selection from animals.
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