WATER STRIDERS
Göran Arnqvist
Umeå 1992
Department of Animal Ecology University of Umeå
S-901 87 Umeå Sweden
AKADEMISK AVHANDLING
som med vederbörligt tillstånd av rektorsämbetet vid Umeå Universitet för erhållande av filosofie
doktorsexamen i ekologisk zoologi kommer att offentligen försvaras fredagen den 23 :e oktober
1992, kl. 1 0 .0 0 i hörsal F, Humanisthuset. Examinator: Prof. Christian Otto, Umeå.
Opponent: Dr. Andrew Sih, Lexington, USA.
ISBN 91-7174-704-4
O rganization
UMEÅ UNIVERSITY
Department of Animal Ecology
S-901 87 Umeå, Sweden
Document name
DOCTORAL DISSERTATION
Date of issu e
October 1992Author
Göran Arnqvist
Ti tle
Sexual selection and intersexual conflicts in water striders
Ab st ract
This thesis deals with evolutionary aspects of the reproductive biology of water striders (Heteroptera: Gerridae), a group o f semi-aquatic insects. The adaptive significance as well as the evolutionary consequences of a number of reproductive behaviours were studied.
Eggs of water striders are parasitized by the parasitic wasp Tiphodytes gerriphagus. Female water striders of some species lay their eggs in groups, whereas others spread out single eggs. A theoretical model was developed to predict the effect of egg laying strategy on the infestation risk. It was predicted that solitary eggs and eggs in large groups should suffer lower infestation risks than eggs in groups of intermediate size. The results of an empirical test of the model were in accordance with the predictions.
Male water striders guard the females after copulation. In a series of experiments, where partly sterilized and normal males were used, it was determined that the last male to mate a multiply mated female fertilized approximately 80% of the female's eggs. The postcopulatory mate guarding behaviour exhibited by males was thus interpreted as a paternity assurance strategy, to avoid sperm competition.
Female water striders are reluctant to mate, and the sexes engage in a precopulatory struggle where females attempt to dislodge males attempting copulation. Males of the water strider Gerris odontogaster are provided with two abdominal processes, which were shown to function as grasping devices during mating. The length of the processes was subjected to intersexual selection in field populations, and the length of the processes was related to a male's ability to endure the precopulatory struggle. Contrary to predictions, the heritability of the processes was high (h2 =1. 01 ± 0.28).
The results of a series of experiments showed that there is a basic conflict of interest between the sexes regarding the mating decision and the mating frequency. While males generally benefit from matings in terms of increased paternity, females experience several costs of mating. Mating females suffered three times as high predation risk as did solitary females, and a lower mobility resulting in time/energy costs. However, mated females did not experience any energetic or genetic benefits from rematings, nor did the females benefit from replenishment of sperm supplies. A theoretical optimization model was developed to predict female reluctance behaviour in a sexual conflict situation, and the predictions were tested empirically. It was concluded that female reluctance during the precopulatory struggle represents a general reluctance to mate (intersexual conflict) rather than an adaptive female mate assessment strategy. Further, female reluctance varied with population density and sex ratio, and this variation was predicted to affect the pattern and intensity of sexual selection.
Estimates of sexual selection were made in field populations with multivariate statistical techniques, and several traits, including parasite load, body size and secondary sexual traits, were found to experience sexual selection. As predicted, the selective regimes varied considerably between different populations, and the importance of spatial and temporal variations in selective regimes is discussed.
Key words
Sexual selection, mating behaviour, parasitism, sperm competition, mate guarding, sexual dimorphism, natural selection, sexual conflicts, water striders, Heteroptera, Gerridae, Gerris, Scelionidae, Trypanosomatidae.
Language
EnglishISBN
9 1.7 1 7 4.7 0 4 . 4Number of pages 95
Signature
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Date
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o n t e n t sList of papers... 4
Introduction...5
Natural history of water striders... 5
Patterns of egg deposition and parasitism...6
Sperm competition and paternity assurance... 7
Intersexual conflicts...8
Conflicts over the mating frequency and the mating decision...8
Precopulatory fighting...9
Sexual selection... 11
The peacock's tail: male abdominal processes... 11
The mechanism of selection: intrasexual selection or female choice?. 12 Good genes or nonadaptive female choice?... 12
The role of parasites... 13
A mechanistic approach: predicting and measuring selection... 14
Local adaptation in metric traits... 15
Concluding remarks and future prospects...16
Acknowledgements... 18
Literature cited...20
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is t o f p a p e r s-This thesis is a summary and discussion of the following papers, which will be referred to in the text by their Roman numerals:
I. Arnqvist, G. and Byström, P. 1991. Disruptive selection on prey group size: a case for parasitoids? American Naturalist 137:268-273.
II. Arnqvist, G. and Mäki, M. 1990. Infection rates and pathogenicity of trypanosomatid gut parasites in the water strider Gerris odontogaster (Zett.)(Heteroptera: Gerridae). Oecologia 84:194-198.
III. Arnqvist, G. 1988. Mate guarding and sperm displacement in the water strider Gerris lateralis Schumm. (Heteroptera: Gerridae). Freshwater Biology 19:269-274.
IV. Arnqvist, G. 1989. Sexual selection in a water strider: the function, nature of selection and heritability of a male grasping apparatus. Oikos 56:344-350.
V. Arnqvist, G. 1989. Multiple mating in a water strider: mutual benefits or intersexual conflict? Animal Behaviour 38:749-756.
VI. Arnqvist, G. 1992. Precopulatory fighting in a water strider: intersexual conflict or mate assessment? Animal Behaviour 43:559-567.
VII. Arnqvist, G. 1992. The effects of operational sex ratio on the relative mating success of extreme male phenotypes in the water strider Gerris odontogaster (Zett.) (Heteroptera: Gerridae). Animal Behaviour 43:681-683.
VIII. Arnqvist, G. 1992. Spatial variation in selective regimes: sexual selection in the water strider, Gerris odontogaster. Evolution 46:914-929.
In t r o d u c t i o n
Ever since Darwin, evolutionary biologists and ecologists have been puzzled by the tremendous diversity and magnitude of sexual dimorphism. Why do males and females typically differ considerably not only in morphology, but also in behaviour during
reproduction? Darwin proposed that such dimorphic traits evolved by sexual selection, which "depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction" (Darwin, 1871, p. 256). Darwin also made a distinction between sexual selection due to male-male competition (intrasexual selection) and sexual selection due to female choice (intersexual selection). But even though some major insights were made early in this century (e.g. Fisher, 1930), it is not until more recently that the topic has received increased attention. The study of sexual selection and the evolution of animal mating systems have experienced a very rapid development during the lasts decades, and has grown to be one of the most vivid and productive areas of evolutionary biology (Bradbury and Andersson, 1987; Harvey and Bradbury, 1991). During this period, several seminal papers have generated bursts of empirical and theoretical attention to various conceptual areas of the topic, some of which I will review briefly below.
This thesis deals with evolutionary aspects of the reproductive biology of water striders, a group of semiaquatic insects. I have focused on two main questions: (/) to assess the adaptive significance of a set of reproductive behaviours, and (ii) to examine the processes and patterns of sexual selection in natural water strider populations. I will start, however, by giving some basic background information about the biology of water striders.
Na t u r a l h i s t o r y o f w a t e r s t r id e r s
The water striders (Heteroptera; Gerridae) form a species-rich but ecologically rather homogeneous group of bugs (Andersen, 1982). They inhabit water surfaces of a range of aquatic habitats both as adults and larvae, and are predators/scavengers feeding mainly on arthropods trapped at water surface film (Jamiesson and Scudder, 1977; Andersen, 1982; McLean, 1989).
In temperate regions, water striders overwinter on dry land as adults in a prereproductive state (Andersen, 1973, 1982). The reproductive activities start in spring after a period of gonad maturation, lasting approximately one to two weeks. Mating and egg laying continue throughout the adult life-span, typically for one to two months, and the life cycles in Fennoscandia are uni- or partly bivoltine (Vepsäläinen, 1974; Vepsäläinen and Patama, 1983;
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Spence, 1989; V). Most water strider species have rather broad habitat requirements and thus occur in a variety of habitats, and several species (3-5) are commonly found in sympatry (Vepsäläinen, 1973; Andersen, 1982; Spence, 1983). The main predators of water striders are invertebrates, such as backswimmers and semi-aquatic spiders, and predators may have considerable impact on the population dynamics as well as the behaviour of water striders (Spence, 1986 a; Zimmermann and Spence, 1989; Sih et al., 1990). Water striders are also exposed to a number of parasites and parasitoids such as egg-parasitic wasps (se below), ecto- parasitic mites, protozoan gut parasites and nematode parasitoids, some of which may cause considerable mortality in natural populations (Spence, 1986 b; Smith, 1989; II; Poinar and Arnqvist, in prep.).
Pa t t e r n s o f e g g d e p o s i t i o n a n d p a r a s it is m
Water striders deposit their eggs on floating objects or submergent vegetation (Andersen, 1982; Spence, 1986 b; I). In order to maximise reproductive success, females face a number of "decisions". Such decisions may concern when and with which male to mate (see below), but a more direct and obvious decision is to deposit the eggs so as to minimise offspring mortality.
A major source of offspring mortality among water striders is egg parasitism by the parasitic wasp Tiphodytes gerriphagus (Spence, 1986 b; Nummelin et al., 1988; I). This parasitoid lays its eggs in water strider eggs, and the wasp embryo develops inside the egg capsule. Parasitism of T. gerriphagus on water strider eggs may be very intense; Spence (1986) reports infestation rates of 80-90 %. Females of some species of water striders tend to aggregate their eggs in groups, whereas other species tend to spread out single eggs (see I, and references therein). In paper I, we developed a general model to predict the effects of grouping on predation risk in situations where the predator/parasitoid consumes a certain number of prey individuals in a group (in effect a form of predator-satiation). The model is primarily based on two statistical effects of group living, namely the avoidance and dilution effects (Turner and Pitcher, 1986), and the results suggests that we would expect disruptive selection on prey group size to arise in situations where e.g. a parasitoid consumes a certain number of insect eggs, larvae or pupae from a group. A general conclusion from the model is that predator-satiating mechanisms seem to generate multiple adaptive peeks with respect to the spatial distribution of prey individuals.
We also performed an empirical test of the model, where water strider egg clusters of different size were exposed to parasitism in the field (I). In general, solitary eggs and eggs in large clusters suffered lower predation risk than did eggs in intermediate cluster sizes. There was a fair qualitative and quantitative agreement between the empirical results and the
predictions of the model (e.g. see I, Fig. 2). Thus, interspecific differences in egg deposition patterns among water striders may represent different behavioural strategies to avoid egg parasitism.
Sp e r m c o m p e t i t i o n a n d p a t e r n it y a s s u r a n c e
A traditional view in sexual selection theory holds that the reproductive success of males is limited by the number of matings they perform, and males should simply try to maximise the number of mates (Darwin, 1871; Bateman, 1948). However, the important component to males is not number of mates per se, but rather the number of fertilised eggs. Parker (1970) pointed out that whenever a female mates with more than one male, sperm from different males will compete over the fertilization of the eggs, and termed this phenomenon sperm competition. Parker (1970, 1974, 1984) also suggested that in many situations, males are selected to prevent other males from mating with the same female (assure paternity), rather than simply trying to maximise the number of mates.
A number of traits are thought to have evolved in the context of sperm competition. Mating plugs, male grasping morphologies, prolonged copulation, and different types of mate guarding behaviour are all thought to be male adaptations to reduce sperm competition (see Parker, 1970; 1984; Thornhill and Alcock, 1983; Smith, 1984). Males of many species of insects exhibit postcopulatory guarding of the female, and thus invest time and energy that could have been used in finding additional mates (Thornhill and Alcock, 1983).
Postcopulatory guarding may function to prevent other males from mating with the same female. However, the adaptive value of guarding depends critically on the degree of sperm precedence (the proportion of eggs fertilised by the last male to mate), and the advantage of mate guarding generally increases with increased sperm precedence (Parker, 1974; 1984).
Water striders typically exhibit postcopulatory mate guarding of considerable duration, males riding passively on the back of the female after copulation (see e.g. Andersen, 1982). Despite the obvious costs to males, this behaviour may be beneficial to males if a high degree of sperm precedence occurs. In paper III, the results of double mating experiments are reported, where virgin Gerris lateralis females were mated with partly sterilized (irradiated) and normal males. According to expectation, the last male to mate with a female fertilized the predominant part of the eggs. The overall magnitude of sperm precedence was approximately 80% (III). The postcopulatory guarding behaviour of G. lateralis, and most probably that of other water strider species as well, should thus be interpreted primarily as a paternity assurance strategy (III; Rubenstein, 1989).
In t e r s e x u a l c o n f l i c t s
Even though it has long been recognized that male and female interests in reproduction may be asymmetrical, the importance of sexual conflicts for the evolution of mating systems and mating patterns has not been fully acknowledged until more recently (Trivers, 1972; 1974; Dawkins, 1976; Parker, 1979; 1984; Hammerstein and Parker, 1987). Sexual conflicts may be defined as situations where there is a conflict between the evolutionary interests of
individuals of the two sexes (Parker, 1979). Sexual conflicts are considered as important evolutionary components in various areas of reproductive biology and a variety of different conflicts may occur, such as conflicts over isogamous or anisogamous reproduction (Parker, Baker and Smith, 1972), over the relative parental investment (Trivers, 1972; 1974), over monogamous or polygamous mating systems (see e.g. Alatalo et al., 1981), over the mating decision and the mating frequency (Parker, 1979; Hammerstein and Parker, 1979) and over sexual cannibalism (Newman and Elgar, 1991; Elgar, in press).
Co n f l ic t so v ert h em a t in g, fr e q u e n c ya n dt h e, m a t in gd e c is io n
A common intersexual conflict concerns the mating decision and the mating frequency. The primary function of copulation for males is to sire offspring, and males can generally increase their reproductive success by mating with many females (Bateman, 1948; Trivers, 1972). For females, the primary function of copulation is to fertilise their ova. If one mating provides females with sufficient sperm, and the male provides little but gametes in mating, there are no obvious reasons why females should benefit from further matings (Daly, 1978; Parker, 1979). A basic conflict over the mating frequency is thus common, and in male-female encounters males may frequently be under selection to mate whereas females may be under selection to refuse mating (Parker, 1979; Hammerstein and Parker, 1987).
Several potential costs may be involved in mating: (1) time and energy costs, (2) increased risk of predation, (3) risk of injury and (4) risk of disease or parasite transmission (Daly, 1978; Thornhill and Alcock, 1983; Lewis, 1987; Amqvist, 1989; Magnhagen, 1991; V). However, a number of potential benefits may balance the costs experienced by females that mate multiply. Mating may; (1) replenish depleted sperm supplies, (2) provide females with nutrients from males, (3) reduce the risk of mortality, (4) be a hedge against genetic defects of previous mates, (5) increase genetic diversity of offspring (Walker, 1980; Thornhill and Alcock, 1983). As pointed out by Parker (1979), it is difficult to demonstrate sexual conflicts because of the difficulty of measuring the various costs and benefits. Hence, empirical evaluations of the cost-benefit balance for females in repeated matings are scarce (Daly, 1978; Walker, 1980; Knowlton and Greenwell, 1984; Eberhard, 1985).
Water striders of both sexes typically mate multiply (e.g. Vepsäläinen, 1974; Wilcox, 1974; Kaitala, 1987; III; V). Since sperm precedence occurs (Rubenstein, 1989; III), remating
is beneficial to males in terms of reproductive success. For females, however, there are no obvious benefits in mating multiply. In paper V, I assess the potential costs and benefits associated with multiple mating in female Gerris odontogaster in a series of laboratory experiments. It was demonstrated that matings entail severe costs to females, mainly in terms of (0 increased risk of predation from predatory backswimmers (Notonectidae) and (ii) a lower mobility when carrying passive males resulting in time/energy costs such as decreased foraging efficiency (see also Fairbairn, [in press], for similar results). However, there were no major balancing benefits to females in mating multiply, either in terms of (z) sperm
replenishment (see also III; Kaitala, 1987; Rubenstein, 1989; for female ability to store sperm), (ii) males transferring nutrients to females, (iii) reduced risk of mortality or (zv) increased genetic diversification of offspring (V). I concluded that females should theoretically mate approximately every 1 0th day for maximal survival and fecundity. However, females of G. odontogaster as well as those of most other water strider species mate much more often, typically several times every day (e.g. Vepsäläinen, 1974; V). The results show that there is a basic intersexual conflict over the mating decision, and suggest that matings in a sense are enforced by males at the expense of fem ales' primary interests (V).
Pr h c o p iil a t o r yf ig h t in g
The precopulatory interactions between the sexes involve components of aggression in many species of insects, where males attempt to overcome female reluctance (Parker, 1979; Thornhill, 1980; Thornhill and Alcock, 1983; Eberhard, 1985; III; IV). In some of these cases the copulations are thought to be enforced by males against the primary interests of females (intersexual conflicts). However, these interpretations are often controversial since the aggressive elements may actually represent adaptive female mate-assessment behaviours, where females choose vigorous males as mates. In order to determine if matings are enforced by males, it need to be demonstrated (1) that male and female interests in mating are in conflict, and (2) that female reluctance represents a general reluctance to mate rather than an adaptive mate-assessment strategy (Thornhill, 1980).
Matings in most species of water striders involve aggressive elements; females typically struggle to dislodge males attempting copulation (e.g. Spence, 1979; Wilcox, 1979;
Wheelwright and Wilkinson, 1985; Fairbairn, 1988; Krupa et al., 1990; Sih et al., 1990; EI; IV; VI). The mating behaviour of G. odontogaster may be seen as typical for most species of water striders. Matings are initiated by males who typically adjust their position according to surface wave vibrations (Wilcox, 1979), and pounce towards and grasp the females and attempt to achieve copula position and genital contact. The females are reluctant to mate and try to dislodge the males primarily by repeatedly performed backward somersaults (IV; V). This precopulatory fight may end with either (z) the male being dislodged or (ii) female reluctance ceasing after a number of somersaults and copulation and subsequent
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postcopulatory guarding following. While previous results demonstrate that male and female interests in mating are in conflict (paper III and V), the ultimate significance of female reluctance and the precopulatory struggle is addressed in paper VI.
As mentioned above, female reluctance in G. odontogaster may represent two
fundamentally different functions. (1) The precopulatory struggle may reflect the intersexual conflict of interests in mating, and females may be reluctant simply to avoid the costs involved with superfluous copulations in general (Parker, 1979; 1984; Hammerstein and Parker, 1987). Females would then be assumed to be 'making the best of a bad jo b '. (2) On the other hand, female reluctance may be a way of assessing the m ales' endurance, choosing vigorous males with 'good genes' as mates. Female reluctance would then represent an adaptive mate assessment strategy (Thornhill and Alcock, 1983). In paper VI, female reluctance at different operational sex ratios and population densities is compared with predictions made from theoretical considerations. An 'econom ic' cost-benefit model (i.e. a cost minimizing model) is developed to predict optimal female reluctance in situations where females are harassed by males. It is demonstrated that females 'making the best of a bad jo b ' (minimizing immediate costs; i.e. energetic and predation risk) are predicted to struggle only to a certain level, and that this level of reluctance should vary with population density and operational sex ratio.
The effects of density and operational sex ratio on female reluctance, mating frequency and mating duration were studied in a laboratory experiment, using a 2 x 3 factorial design (VI). The reluctance of G. odontogaster females decreased as density and operational sex ratio increased, and females mated more frequently in male biased situations (see also VII). Mating duration increased with increasing density and operational sex ratio. The results of the experiments correspond well with the predictions of the model of a sexual conflict over the mating decision, which suggested that females should struggle less intensely before accepting a male as a mate (and consequently mate more frequently) when the density of males is high. In contrast, the predictions from the adaptive assessment perspective were not supported. I concluded that all available information suggests that the primary function of female reluctance in G. odontogaster is simply to avoid costly and superfluous copulations. Still, it could be argued that females are assessing mate quality within certain constraints (e.g. energetic) dictated by factors related to density and/or sex ratio (Janetos, 1980; Parker, 1983). However, as the 'econom ic' model demonstrated, 'good genes' arguments need not be invoked to explain fully both the existence of and variations in female reluctance behaviour. Thus, since the 'econom ic' model offers the most parsimonious hypothesis, there is no reason to believe that any 'good genes' mechanisms are operating. In agreement, Parker (1984) argued that female mating patterns are more likely to be formed by environmental pressures (i.e. time or energy waste) than by factors related to the genetic quality of their potential mates.
Se x u a l s e l e c t i o n
Sexual selection may be defined as a process, generating a variance in reproductive success among individuals (typically males) in a pattern which is nonrandom with respect to phenotypes. A less formal definition may be: sexual selection is acting whenever there is a relation between a trait (e.g. body size) or a set of traits and reproductive performance (i.e. mating success)(cf. Endler, 1986). With these operational definitions, sexual selection only describes a pattern within a population, and sexual selection is usually further divided into two categories based on the underlying process. These are: (1) intrasexual selection, where members of one sex (usually males) compete with each other over access of individuals of the other sex, and individuals who possess certain traits are more successful in outcompeting others, and (2) female choice (intersexual selection), which is operating whenever females have some behaviour or structure which cause them to bias matings in favour of certain male phenotypes (Halliday, 1983; Kirkpatrick, 1987; Maynard Smith, 1987). In either case sexual selection tends to generate the evolution of sexually dimorphic traits, such as elaborate plumage in birds, horns and antlers in mammals, horns in scarabid beetles, sexual
dimorphism in body size etc. However, it is often very difficult to empirically determine the relative extent to which each process has been involved in the evolution of dimorphic traits, and to further complicate the matter intrasexual selection and female choice may act simultaneously (e.g. Moore, 1990; Harvey and Bradbury, 1991).
Th ep e a c o c k st a il: m a l ea b d o m i n a lp r o c e s s e s
Water striders in general do not exhibit any extraordinary sexual dimorphism (Andersen, 1982). A few exceptions occur, such as the genera Rheumatobates and Ptilomera
(Hungerford and Matsuda, 1965; Eberhard, 1985). Further, there is generally a slight sexual size dimorphism, females being somewhat larger than males (Fairbairn, 1990).
The species G. odontogaster exhibits a sexual dimorphism which is unique among temperate water strider species; males are provided with two abdominal processes situated on the ventral surface of the seventh abdominal segment (see Fig. 1, IV). Several of the papers on which this thesis is based to some extent concern the functional significance and evolutionary dynamics of these male abdominal processes (IV; VII; VIII).
In paper IV, the functional significance of male abdominal processes was studied by freezing a number of mating pairs instantaneously with liquid nitrogen (-195°C), and subsequently photographing the pairs in a scanning electron microscope. The results showed that males used the abdominal processes to hook the females" abdominal tip. The processes
thus functioned as a grasping apparatus, providing males with a posterior attachment to females during mating.
The MECHANISMS SELECTION : INTRASEXUAL SELECTION OR FEMALE CHOICE?
Studies of sexual selection typically focus on patterns rather than processes. A consequence of this research strategy is that, although many studies have demonstrated that sexual selection is an important form of selection, most studies cannot say why sexual selection occurs - i.e. the mechanism of selection is not known (Endler, 1986; Grafen, 1987; Wade and Kalisz, 1990).
Morphological traits in insect males which keep the sexes together during mating (i.e. different forms of grasping morphologies of male tarsi, femora, antennae etc) are traditionally seen as adaptations to reduce intrasexual competition by preventing take-overs (Parker, 1970;
1984; Thornhill, 1984; Eberhard, 1985). By grasping a female efficiently, males avoid being displaced by other males which may inseminate the same female. We would thus predict that the male abdominal processes in G. odontogaster should function to avoid sperm competition via take-overs. However, G. odontogaster males do not attempt take-overs; take-overs have never been observed either in the field or in the laboratory (IV). This implies that take-over avoidance (intrasexual selection) is not an important function of the abdominal processes. In contrast to the traditional hypothesis, it was demonstrated in a series of laboratory
experiments (paper IV) that (1) males with grasping apparatuses that had been made
inoperative experienced a drastic reduction in mating success since they were dislodged more easily by the females during the precopulatory struggle, and (2) the length of the processes was related to a m ale's ability to endure female reluctance during the precopulatory struggle - males with longer abdominal processes were better able to endure female somersaulting behaviour (IV). These results demonstrate that the function of the processes is intersexual rather than intrasexual. Further, sexual selection for long abdominal processes was demonstrated in a field population, where mating males had significantly longer processes than non-mating males (IV).
'Female choice' may seem an inappropriate term for the reluctance behaviour of G.
odontogaster females. However, since females (due to their reluctance behaviour) bias
matings towards males with long abdominal processes (IV; VIII), the selective process is, 'by definition', sexual selection by female choice (IV, cf. definitions by: Halliday, 1983;
Kirkpatrick, 1987; Maynard Smith, 1987).
Go o dg e n e so rn o n a p a p t i v ef e m a l ec h o ic e?
The two fundamentally different views of the female reluctance behaviour of G. odontogaster discussed in paper VI (see above), correspond in several ways to a current controversy regarding sexual selection by female choice. Sexual selection by female choice involves two
components; a male trait and a female mating preference regarding this trait (e.g. Darwin, 1871; Kirkpatrick, 1987). The current view of sexual selection by female choice may be divided into two major schools (see Bradbury & Andersson, 1987; Kirkpatrick, 1987; for reviews). The 'good genes' school postulates that female preferences evolve under selection for females to mate with ecologically adaptive male genotypes. In contrast, the 'nonadaptive' school holds that preferences evolve for other reasons, and that selection often will cause males to evolve maladaptively with respect to their ecological environment. Kirkpatrick (1987) emphasised that information on the male trait only is insufficient to resolve the controversy over female choice, and that more effort should be made to understand the mechanism and evolution of the female preference (see also Sullivan, 1989).
Since female reluctance is the mechanism of female choice in G. odontogaster, one may ask whether female reluctance represents an adaptation for choosing vigorous males with good genes as mates or if the bias in matings merely is a side-effect of, in this case, a sexual conflict? As concluded in paper VI, females struggle to avoid costly matings in general rather than to assess the mate's genetical quality, which strongly suggests that female mating preference is a by-product of evolutionary forces unrelated to intraspecific mate
discrimination. Sexual selection by female choice in G. odontogaster should thus be seen as a side-effect rather than the ultimate cause of the reluctance, and would hence represent a case of 'nonadaptive' female choice (Kirkpatrick, 1987).
t h e r o l e q e p a r a s it e s
Due to the rev o lu tio n ary relationship between parasites and hosts, parasites have received a large amount of attention in recent theoretical and empirical studies of intersexual selection (Hamilton and Zuk, 1982; Bradbury and Andersson, 1987; Read, 1988; McLennan and Brooks, 1991). Hamilton and Zuk (1982) proposed that male freedom from parasites and diseases should be important traits in the evolution of female mating preferences. They suggested that females should prefer mating with males with low parasite loads, since this would increase the offspring fitness provided that parasite resistance has genetic components. The theory thus belongs to the "good genes" type of models of female choice. A number of studies in a wide variety of species have demonstrated that sexual selection for parasite freedom in males does occur (Read, 1988). However, as stressed by Kirkpatrick (1987; pp. 49-50), information about the male trait alone is insufficient in order to understand the evolution of female mating preferences, and it has proven to be extremely difficult to separate causes and effects with regard to sexual selection for parasite free males (see McLennan and Brooks, 1991; for a critique).
Water striders of many different species are parasitized by protozoan gut parasites. These parasites belong to the family Trypanosomatidae, and they infect their hosts by ingestion. Paper II provides the first study of the pathogenicity of trypanosomatid parasites in water
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striders. The infection rates were shown to be very high in natural populations of G.
odontogaster during the reproductive season. In a number of laboratory experiments, it was
demonstrated that these parasites are indeed pathogenic to their hosts. Infections reduced the overall vigour of adult G. odontogaster males, and infections caused increased host mortality during food stress (II).
Provided that there is a genetic component in trypanosomatid parasite resistance, choosing parasite free males could potentially represent adaptive female choice. Indeed, in paper VIII, where sexual selection was measured in three natural populations of G.
odontogaster, it was demonstrated that rather intense sexual selection for parasite free males
do occur (see VIII fig. 1, and below). However, as argued in paper VI, the mechanism of female choice in G. odontogaster (female reluctance to mate) is due to factors related to the costs of mating rather than mate assessment and adaptive mate choice. This strongly suggests that female choice of parasite free males in G. odontogaster is a side-effect rather than a causal evolutionary factor of female mating preferences, and hence does not lend support to the hypothesis of Hamilton and Zuk (1982).
A MECHANI5.1ICAEPRQACH PRE_pICI MjAND MEASURING SELECTION
The study of phenotypic selection in natural populations has been given considerable attention in recent years. Multivariate methods have been developed for measuring selection in natural populations when selection acts simultaneously on a set of phenotypically correlated characters (Lande and Arnold, 1983; Manly, 1985; Endler, 1986), and for analyzing temporal variation in selection by partitioning the total effect of selection into several selection episodes related to different fitness components (Arnold and Wade, 1984a,
1984b; Conner, 1988; Moore, 1990). Although a large number of empirical studies have demonstrated selection in natural populations, the mechanisms of selection are known only in a few cases (see Endler, 1986; for a review). Recently, several authors have stressed that a correlational approach is insufficient for inference of causal patterns of selection, and that a more mechanistic approach (i.e. a thorough knowledge of the ecology and genetics of the study organism in concert with studies of selection) may provide new perspectives in evolutionary biology, e.g. a priori predictions about the outcome of selection and about the factors affecting the mechanisms of selection (Endler, 1986; Grafen, 1987; Mitchell-Olds and Shaw, 1987; Wade and Kalisz, 1990; VIII).
In paper VI, I demonstrated that G. odontogaster females became less reluctant to mate as the operational sex ratio and population density increased. This pattern has also been found in G. buenoi by Rowe (in press). Since female reluctance is an important mechanism of sexual selection in G. odontogaster, we would expect the intensity or strength of selection to be negatively correlated to sex ratio and density. This general prediction is addressed in papers VII and VIII, using an experimental (VII) and an observational (VIII) approach.
The relation between the strength of selection and operational sex ratio was tested in a field enclosure experiment (paper VII), where males with short and long abdominal processes were allowed to compete for matings at different sex ratios. It was demonstrated that the relative importance of long processes in terms of acquiring matings was highest in female biased situations, and that it decreased with increasing sex ratio as predicted. Thus, in contrast to general theory, which states that the intensity of sexual selection should increase with increasing sex ratio (Wade and Arnold, 1980; Sutherland, 1987), the intensity of sexual selection for long abdominal processes in G. odontogaster was negatively correlated with sex ratio. Further, female mating frequency increased with increasing sex ratio.
In paper VIII, the sexual selection regimes in natural populations of G. odontogaster were compared with a priori predictions of selection. Since females are less reluctant to mate and thus less discriminative under high population density, selection was predicted to be inversely density dependent. Sexual selection was measured in three populations with large differences in population density. Standard univariate and multivariate methods were used (Lande and Arnold, 1983), and estimates of selection were made on a number of
morphological traits. Mating and solitary males were sampled in the field, and ten linear measurements were subsequently made on each individual. In addition, the intensity of trypanosomatid gut parasite infections was determined.
Parameter estimation in subsequent selection analysis was made with univariate and multivariate linear regression techniques, while tests of significance were made with
generalized linear models (probit regression)(see VIII). A number of traits, including parasite load, body mass, body size and male abdominal processes, were found to experience
significant sexual selection. Further, the investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, the patterns of selection corresponded well with the predictions; sexual selection was more intense in the low density populations, and this pattern was especially pronounced for traits reflecting male grasping ability and endurance during the precopulatory struggle (e.g. abdominal process length).
Lo c a la d a p t a t i o ninm e t r ict r a it s
In studies of evolutionary biology, it is critical to distinguish between selection and evolutionary response to selection (Lande and Arnold, 1983; Arnold and Wade, 1984a). Selection can be measured and described purely in terms of phenotypes, whereas evolutionary response to selection depends on the nature of genetic variation. If a certain trait in a
population experiences phenotypic selection and the trait variation has additive genetic components, a change in the gene frequencies in the population may be the result, provided that evolutionary constraints do not prevent local adaptation (Grant and Price, 1981;
16
sufficiently different (different genotypes are favoured by selection), selection may lead to adjacent populations being locally adapted (i.e. having dissimilar gene pools). In this
scenario, a moderate gene flow between populations would further the maintenance of genetic variation (Felsenstein, 1976; Endler, 1977; Nevo, 1978; Hedrick, 1986). Thus, in order to demonstrate local adaptations it must be shown that (1) natural populations differ with respect to genotype frequencies, and that (2) these differences are the result of selection rather than random processes. The genetic differentiation among local water strider populations is generally high (as demonstrated by enzyme gene variation; i.e. Varvio-Aho and Pamilo, 1981; Varvio-Aho and Pamilo, 1982; Preziosi and Fairbairn, 1992). However, it is not known whether this variation represents local adaptation or is result of random processes (genetic drift). In any case, these studies indicate that gene flow between water strider populations may be limited, allowing different populations to adapt to local selective regimes (Blanckenhorn, 1991; Preziosi and Fairbairn, 1992).
The populations of G. odontogaster studied in paper VIII differed significantly both in sexual selective regimes and in mean phenotypes. It is, however, very difficult to assess to what degree the observed phenotypic differences among males also represent genotypic differences (Grant and Price, 1981), even if several of the traits are known to have additive genetic components in trait variation (Arnqvist, 1990). Nevertheless, one of the traits merits a closer examination. In paper IV, it was demonstrated that the length of male abdominal
2
processes was highly heritable (heritability estimate h = 1.01 ± 0.28). The observed differences in process length between the populations should thus to some extent represent local adaptations. In support of this suggestion, the relative lengths of processes in the populations were in accordance with expectations; abdominal processes were longest in the population where selection for long processes was strongest, and processes were shortest in the population where selection was weakest. Further, selection does not only affect the phenotypic mean, but also the phenotypic variance. In general, selection tends to decrease trait variability (Grant and Price, 1981; Endler, 1986). Again, in accordance with
expectations, the population that experienced no selection for abdominal process length exhibited highest trait variance. Since there is some gene flow between G. odontogaster populations during spring dispersal (Vepsäläinen 1974), genotypic exchange between locally adapted populations with different selective regimes may contribute significantly to the maintenance of additive genetic variation for length of abdominal processes.
Co n c l u d i n g r e m a r k s a n d f u t u r e p r o s p e c t s
The main theme of this thesis has been to understand the processes involved in sexual selection in water striders (II; III; IV; V; VI), and to describe the patterns and effects of
selection in natural populations (IV; VII; VIII). As stressed by Endler (1986), understanding the mechanisms of selection is of vital importance in studies of evolutionary ecology. Further, assuming constant relative fitness of phenotypes is invalid and constitutes an example of typological thinking in biology (Endler, 1986). Selective regimes and optimal phenotypes typically vary both spatially and temporally (e.g. Falconer, 1981; Endler, 1986; Anholt, 1991; Jones et al., 1992).
It is very difficult to attain a satisfactory understanding of the mechanisms of selection in specific systems (Harvey and Bradbury, 1991), not to mention all potential factors that might influence the intensity of selection and the effects of selection in natural populations. However, the studies where this has been at least partially achieved (including studies of
Cepea [Cain and Sheppard, 1954; Cain, 1983], Poecilia [Endler, 1983] and Geospiza [Grant
and Price, 1981; Price et al., 1984]) suggest that a mechanistic approach should be adopted (Endler, 1986). Experimental studies of the biology of the organism (in terms of e.g. ecology, behaviour and genetics) performed at the individual level, should form the basis for
observational and experimental studies at the population level (Grant and Price, 1981; Endler, 1986; Wade and Kalisz, 1990). Such a research strategy, where experimental studies
addressing processes and observational studies addressing patterns act in concert, should prove to be a rewarding avenue of research in evolutionary ecology.
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Ac k n o w l e d g e m e n t s
This thesis would never have been accomplished without the intentional (and unintentional!) support of many, many people. Firstly, I'm tremendously grateful to my parents for
continuous support during my early (and later!) years, and for not laughing at me when I first stated (six years old) that I was going to be a zoologist. I'm also most grateful to my
supervisor Christian Otto, for not laughing at me when I somewhat later again suggested that I would like to be a zoologist. Christian has provided continuous encouragement and
enthusiastic support during the years this thesis was written. I also owe Christian many thanks for his willingness to discuss almost anything, for his remarkable ability to fill preliminary drafts of manuscripts with red ink, and for his financial support without which several of the studies on which this thesis is based would never have been performed!
Perhaps the most important factor for successful science is social atmosphere. Science is a creative process, and it has to be fun to go to work! I wish to thank all my colleagues and friends at the Department of Animal Ecology, mentioned and unmentioned, for creating such a friendly, warm and unimpeded atmosphere! Special thanks to: Göran Andersson for the coffee breaks and for being our private party-pro. Gunnar Borgström and Stig-Ola Ivarsson for providing skilful technical assistance. Lena Burström for always being happy to help out. Per Byström, who really is from Kiruna, for fruitful collaboration. Bent Christensen for never beating me in table-hockey. Sebastian Diehl for being an unusual connoisseur of the noble art of living and a very dear friend. Peter Eklöv for scuba diving for pikes (!) and for always looking at things from the bright side of life. Johan Elmberg for once doing sexual selection. Göran Englund for setting the morning habit standards. Frank Johansson for the birds and the laughter, and for slamming me back to earth. Kjell Leonardsson for giving good advice at the right time. Görel Marklund for her excellent drawings, and for being so generous. Mari Mäki for her patience and all the delicious calories. Anders Nilsson for being mysteriously devoted to beetles and weird music, but most of all for once telling me that water striders must be the optimal research organisms! Tarja Oksanen for being happy. Tommy Olsson who introduced me into behavioural ecology. Lennart Persson for being so uncompromisingly fond of science and Björklöven, and for his aberrant sense of humour. Göran Sjöberg for sharing all the paragraphs in the board with me. Olle Söderström for the beers and the memories, and for having the ability to brighten up a dull day. And finally, a special thank to the floor-ball gang, for the weekly adrenaline-chock and all the scars and wrecked ankles and without which Mondays would not have been the best day of the week ....
Several people provided assistance with various experiments; the help of M. Arnqvist- Bonta, G. Englund, H. Fängstam, F. Johansson and M. Mäki is gratefully acknowledged. Also, a large number of people that have provided invaluable and constructive comments on various drafts of the papers owe recognition: J. Alcock, B. Anholt, J. Arnold, H.J. Brockman, S. Diehl, J. Elmberg, D.J. Fairbairn, B. Giles, K. Leonardsson, C. Otto, L. Persson, L. Rowe, J.R. Spence, R. Thornhill, K. Vepsäläinen and R.S. Wilcox.
I also wish to forward a special thank to Karin Ekström and the staff at the Drosophila Stock Centre at the Department of Genetics, for providing me (or more specifically; the water striders) with food for the experiments. Without your generosity, the experiments would have been far more time-consuming...
Finally, my deepest gratitude to Maja and Nina, for your love and support, and for unintentionally forcing me to see things other than science in life.
This thesis was financially supported by The Swedish Natural Science Research Council (through grant to C. Otto), The Royal Swedish Academy of Sciences, 'Gustaf och Hanna Winblads minnesfond', 'K-fonden', 'JC Kempes minnes stipendiefond', 'Stiftelsen Kungaparets stipendiefond' and the Wenner-Gren Centre Foundation.
20
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