New Results

Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon

William Toubiana, Abderrahman Khila
doi: https://doi.org/10.1101/430314

Abstract

Sexually selected traits can reach high degrees of expression and variation under directional selection. A growing number of studies suggest that such selection can vary in space, time and form within and between populations. However, the impact of these fluctuations on sexual trait expression is poorly understood. The water strider Microvelia longipes displays a striking case of exaggeration and phenotypic variation where males display extreme differences in the size of their rear legs. To study the origin and maintenance of this exaggerated trait, we conducted comparative behavioral and morphometric experiments in a sample of Microvelia species. We uncovered differences both in the mating behavior and the degree of sexual dimorphism across these species. Interestingly, M. longipes evolved a specific mating behavior where males compete for egg-laying sites, consisting of small floating objects, to intercept and copulate with gravid females. Field observations revealed rapid fluctuation in M. longipes habitat stability and the abundance of egg-laying sites. Through male-male competition assays, we demonstrated that male rear legs are used as weapons to dominate egg-laying sites and that intense competition is associated with the evolution of rear leg length exaggeration. Paternity tests using genetic markers demonstrated that small males could only fertilize about 5% of the eggs when egg-laying sites are limiting, whereas this proportion increased to about 20% when egg-laying sites become abundant. Furthermore, diet manipulation and artificial selection experiments also showed that the exaggerated leg length in M. longipes males is influenced by both genetic and nutritional factors. Collectively, our results highlight how fluctuation in the strength of directional sexual selection, through changes in the intensity of male competition, can drive the exaggeration and phenotypic variation in this weapon trait.

Introduction

Phenotypic variation is central to the process of evolution [1], and understanding the mechanisms of its emergence and persistence in natural populations remains at the forefront of evolutionary biology studies [2], Sexually selected traits represent some of the primary examples illustrating both intra- and interspecies phenotypic variation [3, 4], Males in both vertebrates and invertebrates are known to wield extravagant phenotypes that can differ in their nature, location, size, and shape [3-5]. Examples include deer antlers, beetle horns, eyestalks in some flies, pseudoscorpion antennae and harlequin beetle legs. Some males of these species can develop degrees of trait expression so high that they appear exaggerated compared to other body parts or other homologous structures in the other sex [6]. A central prediction for these exaggerated traits to evolve is that only large individuals can afford to bear them, which can be a good indicator of body size and thus act as an honest signal for male quality [7–9]. Under this prediction, females will favor males with the highest trait expression, thus imposing strong directional selection in favor of trait exaggeration [3, 10]. In other situations, the trait is used as a weapon in male-male competition with its size being a good predictor for the outcome of the contest over access to females [11–14].

In these examples, sexual selection is thought to be directional and persistent over time [9, 12, 15]. These traits are also known to be subject to survivorship costs, which constrain their degree of expression resulting in a net stabilizing selection. These observations raise important questions regarding the maintenance of phenotypic variation in natural populations [3, 9, 15–21], A growing number of studies suggest that selection may not be as consistent over time and space, and that environmental changes may influence the strength, direction, and form of sexual selection [22–26], These fluctuations in selection may, in turn, favor the elevated plastic response and genetic variation observed in sexual traits, possibly influencing their variation and evolution over time [9, 21–23], Studies assessing the interplay between selection, genetics and plasticity, within the context of a changing environment are therefore crucial to the general understanding of the origin and maintenance of highly variable exaggerated sexual traits.

Here we focus on a novel model system, the water strider Microvelia longipes, that displays a strong sexual dimorphism where males have evolved both longer and more variable rear legs than females [27], The genus Microvelia (Heteroptera, Gerromorpha, Veliidae) comprises some 170 species of small water striders distributed worldwide and occupying various fresh water habitats including temporary rain puddles and stable large water bodies [27], First we reconstructed phylogenetic relationships of five Microvelia species and compared their degree of dimorphism, scaling relationships between leg and body length, and various aspects of mating behavior. We report a clear association between the intensity of male competition and the evolution of trait exaggeration in M. longipes males. We then determined the fitness advantages of these exaggerated legs through fertilization success performed under selective conditions reflecting fluctuations in their natural environment. Finally, we assessed the contribution of the strength of sexual selection, genetic variation, and phenotypic plasticity to the variation of exaggerated rear legs in M. longipes males.

Results and discussion

Sexual Dimorphism and scaling relationships in Microvelia species

We found a considerable inter-species variation in the degree of sexual dimorphism within the Microvelia genus (Figure 1). Measurements of various body parts revealed dimorphism in average body length, leg length, and the scaling relationship between these two traits (Figure IB; Supplementary table 1). In some species, such as M. americana and M. paludicola, the dimorphism in leg and body length is small, whereas in others such as M. longipes, the dimorphism is spectacular (Figure 1A). The extreme leg elongation found in M. longipes males originates from the evolution of hyperallometry where the allometric coefficient is significantly higher than 1 and reaches a value of 3.2 - one of the highest known (Figure 1B; Supplementary table 1) [5, 28]. In contrast, M. longipes females and both sexes of all other species show scaling relationships between leg and body length that are isometric or near isometry (Figure 1B; Supplementary table 1). Taking the two traits individually, M. longipes male legs are both significantly longer and more variable than female legs (Figure 2A, B; Supplementary table 1). In contrast, M. longipes body size is significantly more variable in males than in females, but average body length is not significantly different between the sexes (Figure 2A, C; Supplementary table 1). Despite these major differences, both sexes presented leg and body length distributions that were not significantly different from normality (Supplementary table 2).

Figure 1:
Figure 1:

Diversity in leg sexual dimorphism and mating behaviours in Microvelia. A) Phylogenetic relationships between five Microvelia species using Maximum Likelihood and Bayesian analyses. Support values obtained after Bayesian posterior probabilities and 1000 bootstrap replicates, respectively, are shown for all branches. Pictures of males (right) and females (left) illustrate divergence in sexual dimorphism in the five Microvelia species. Scale bar represents 1mm. B) Scaling relationships of log-transformed data between rear legs and body lengths were estimated in males (blue) and females (red) of the five Microvelia species using Major Axis regressions. The equations and fitting (R-squared) of the linear regressions in males and females were indicated using the same colour codes. C) Behavioural characters describing the mating system of the five Microvelia species. These characters were mapped onto the phylogeny based upon the parsimony criterion.

Figure 2:
Figure 2:

Phenotypic variation of rear leg exaggeration and body length in M. longipes. A) Phenotypic variation of rear leg length in males and in a female. (B) Rear leg length and (C) body length distributions of males (white) and females (grey) from a natural population collected in French Guyana.

Finally, we found that the males of three Microvelia species (Microvelia sp., M. americana and M. paludicola) evolved prominent spikes on the rear legs indicative of a function in grasping females during pre-mating struggles [29] (Figure 1A). Overall, these analyses indicate that the evolution of hypervariable exaggerated legs in M. longipes males results from the high variance in body length and the associated hyperallometric relationship with leg length (Figure 1 and 2). In M. pulchella, despite the high variation in male body length, the near isometric relationship between leg and body length makes their legs less exaggerated and less variable than M. longipes males (Figure 1B; Supplementary table 1). Moreover, the diversity in sexual dimorphism between Microvelia species does not seem to follow any particular phylogenetic pattern (Figure 1), suggesting that variation in the ecology, behavior, or mating systems may play a role in the divergence of the sexes in these species.

Mating systems in Microvelia species

We characterized mating systems and sexual interactions in all five species to better understand the differences in sexual dimorphism (Supplementary figure 2). In nature, the Microvelia genus comprises species that occupy a wide variety of habitats [27], Most species live nearshore, in stagnant, large water bodies [27], Some species, like M. longipes, M. pulchella or Microvelia sp. are gregarious and specialize in small temporary puddles filled with rainwater in tropical South America [27, 30]. Behavioral observations both in the wild and in laboratory-recreated puddles revealed that M. longipes males are highly territorial and tend to aggressively guard floating objects consisting of small twigs or pieces of dead leaves (Supplementary figure 3). These are egg-laying sites where males signal to attract females, by vibrating their rear-legs and pounding with their genitalia on the water surface producing ripples (Supplementary videos 1 and 2). We hereafter refer to these objects as egg-laying floaters. When a female approaches the floater, the dominating male switches from signaling to a courtship behavior. The female inspects the floater and either leaves or mates without any resistance with the courting male and immediately lays 1 to 4 eggs (n=26 mating events) (Supplementary figure 3; Supplementary video 2). The male then initiates an aggressive guarding behavior by turning around the egg-laying female and chasing other approaching males to (Supplementary video 2). After egg-laying the female leaves and the male initiates another cycle of signaling on the same floater. During this entire process, other males constantly challenge the signaling male in an attempt to dominate the floater. During these contests, the dominant and the challenging male fight back-to-back by kicking each other with their rear-legs until one of them is chased away (Supplementary video 2). We also observed that females could lay eggs in the mud at the margin of the puddle and that males attempt to mate outside floaters by jumping on female’s back randomly in the puddle.

M. pulchella, the sister species of M. longipes (Figure 1A), is also found in small temporary puddles [30] and displays a highly similar mating behavior despite the lack of rear-leg exaggeration (Figure 1C). Males of M. pulchella compete for egg-laying floaters, fight with their rear-legs, and generate ripples to attract females. Also like M. longipes, females of M. pulchella lay their eggs both on floaters and in the mud. In spite of similarities in their mating behavior, these two sister species display significant morphological differences, raising the question as to which factors drove the evolution of trait exaggeration in M. longipes.

In the three other species, M. americana, M. paludicola, and Microvelia sp., males possess grasping spines on their rear-leg femurs (Figure 1A) and actively harass females in an attempt to mate. Females consistently struggle through vigorous shaking, frequently resulting in the rejection of the male. Males of these three species also fight occasionally but the fights do not seem to result in the dominance of any particular localized resource (Figure 1C; Supplementary figure 2). M. americana and M. paludicola females lay eggs exclusively on water margins while females in Microvelia sp. lay eggs randomly either on floaters or water margins, but do not do so immediately after mating (Figure 1C; Supplementary figure 2). Altogether, these data show that the behavior, consisting of contests using the rear-legs, predates the origin of exaggerated leg length and could therefore be necessary but not sufficient for its evolution. Moreover, differences in egg-laying habits may have driven the diversity in male mating strategies and sexual dimorphism in the Microvelia genus. In small temporary habitats, eggs laid in the mud are at high risk of desiccation when water levels go down, and nymphs tend to drown at hatching when water levels go up, something we frequently observe in laboratory conditions. Egg-laying behavior on floating objects, which remain on the surface despite fluctuating water levels, is likely an adaptation to the fast-changing state of the habitat. Interestingly, male behavior consisting of dominating these egg-laying floaters is observed only in species where females lay eggs just after mating, indicative of the high fitness value in accessing them. This behavior is also associated with the high body length variation in M. longipes and M. pulchella males (Figure 1B), suggesting a link between body size variation and competition for oviposition sites.

Intensity of male competition in M. longipes compared to M. pulchella

In order to evaluate the contribution of exaggerated leg length to male mating success, we tested whether a correlation existed between male leg length and their ability to dominate egg-laying sites. We found increased rear leg length to be strongly correlated with the fighting outcome (ANOVA, F(l, 13) = 144.6, p < 0.01), where the males with longer legs won 97% of the fights (n= 75 fights) and dominated the floater (Figure 3A). We also observed this male dominance over egg-laying sites in M. pulchella, which did not evolve leg exaggeration. We therefore hypothesized that male phenotypic differences between M. longipes and M. pulchella could be driven by differences in the intensity of male competition. When we measured the intensity of male competition in standardized space conditions, we found that M. longipes males fought on average 8 times more frequently than M. pulchella males in a period of 1 hour (Figure 3B, Supplementary table 3). This indicates that male competition is significantly higher in M. longipes than in M. pulchella. More importantly, 81 % of M. longipes fights occurred on the floaters (Figure 3B, Supplementary table 3) whereas M. pulchella males’ fights occurred randomly on and away from floaters (Figure 3B, Supplementary table 3). The same result was reached when we repeated this experiment in standardized density conditions taking into account size differences between the two species (Supplementary table 3). These data demonstrate first that increased rear leg length in M. longipes males favors male dominance over egg-laying sites to better intercept gravid females. While both M. longipes and M. pulchella males intercept females and compete on those egg-laying sites, competition intensity for egg-laying sites is almost an order of magnitude higher in M. longipes. A primary difference between the ecology of these two species is that M. longipes specializes in rainwater-filled small puddles while M. pulchella is a generalist that can be found in both temporary and more stable water bodies ([31, 32] and personal field observations). This difference in niche specialization has two major impacts on M. longipes population structure. First, M. longipes populations can reach very high densities confined in a small space, something we observed frequently in the wild and which is not the case for M. pulchella. Second, because the water level in the puddle can change rapidly (Supplementary figure 4), floaters represent the safest substrate in terms of survival of the progeny. This may explain why females bounce the floater up and down before they copulate and lay eggs (Supplementary video 2), and why M. longipes males are so aggressive in dominating these floaters. The situation is different for M. pulchella due to the higher stability of the habitat, making floaters less critical and the survival of eggs in the mud more likely. These ecological conditions favoring high-density populations and floating objects as the more suitable egg-laying substrate may have at least contributed to the high competitiveness observed in M. longipes, and thus acted as a driving force for the evolution of the exaggerated leg length for use as a weapon. Both empirical and theoretical models suggest that population density can influence aggressiveness and the intensity of sexual selection [33], and our data show how increased competitiveness can drive secondary sexual traits to reach dramatic levels of expression.

Figure 3:
Figure 3:

Selective pressures and reproductive fitness of leg exaggeration in M. longipes males. A) Relationships between fighting outcome and male rear leg length. Winners correspond to males keeping the access to the egg-laying sites after the fights. Solid line represents a fitted linear regression model, B) Frequency of fights between M. longipes and M. pulchella on both floaters and outside floaters, C) Fertlization success of large and small males and the contribution of egg-laying sites. Heterozygous eggs result from the siring of short-legged males (short-legs selected line) and females (long-legs selected line). Homozygous eggs result from the siring of long-legged males (long-legs selected line) and females (long-legs selected line). The table summarizes an ANOVA test recapitulating the influence of the floaters and the egg-laying locations on the egg genotypes.

Effect of exaggerated leg length on male reproductive fitness in M. longipes

Post-mating competition is widespread in insects [34], including water striders [35,38], and can strongly alter the outcome of pre-mating strategies [34, 39]. Field observations also indicate that the state of the habitat occupied by M. longipes can fluctuate rapidly and, sometimes, the water can evaporate entirely in days (Supplementary figure 4). Moreover, the amount of egg-laying resources is highly variable from one puddle to another and can additionally fluctuate with water level (personal observations from the field). We hypothesized that these rapidly changing conditions will influence competition and mating success across the distribution of male phenotypes. To test this hypothesis, we conducted paternity tests using M. longipes lines that are homozygous for distinct microsatellite markers that can reveal the identity of the parents (see methods for more details). We set the experiment such that heterozygous progeny could only originate from eggs fertilized by small males. Because egg-laying floaters represent the primary resource that males dominate to intercept gravid females, we designed a first treatment where floaters were limiting (3 floater for 6 large and 6 small males) and another treatment where floaters were abundant (20 floaters for 6 large and 6 small males). We also genotyped the progeny from eggs laid in the mud to determine mating success of different male phenotypes in contexts other than the dominance of floaters. In all replicates of each treatment, females laid the majority of their eggs on floaters regardless of whether floaters are limiting (91% of a total of 512 eggs) or abundant (71% of a total of 500 eggs) (Figure 3D). However, females laid on average three times more eggs on the mud when floaters were limiting (Supplementary table 4). In the condition where floaters were limiting, small males fertilized 4.6% (15 eggs of a total of 357 eggs) of the eggs laid on floaters and 25% of the eggs laid in the mud (35 eggs of a total of 143 eggs) on average (Figure 3D; Supplementary table 4). Interestingly, the number of eggs sired by small males was more than twice higher in the mud than on floaters (Figure 3D; Supplementary table 4). This suggests that when the dominance of floaters by small males is limited, they primarily achieve egg fertilization by mating outside floaters. In the condition of abundant floaters, the proportion of eggs fertilized by small males on floaters increased significantly to 19% (96 eggs of a total of 468 eggs) (Figure 3D; Supplementary table 4), while that outside floaters remained unchanged (11 eggs of a total of 44 eggs) (Figure 3D; Supplementary table 4). In contrast to the treatment with limiting floaters, here the number of eggs fertilized by small males is almost nine times higher on floaters than in the mud (Figure 3D; Supplementary table 4). These results show that small males can sire significantly more progeny when egg-laying sites are abundant but can also mate outside these egg-laying sites when floaters are limiting. Therefore, sexual selection is strong in favor of large males with long legs but can become relaxed in conditions where egg-laying sites are abundant. Rapid changes in water level and high heterogeneity between puddles are intrinsic to the life history of this species and are expected to cause variation in the amount of accessible egg-laying floaters over time and space. This fluctuating selection is therefore likely to influence the strength of competition and mating success and contribute to the high phenotypic variation found in M. longipes natural populations.

Environmental and genetic contributions to male rear leg variation

We have shown that possible fluctuation in the strength of sexual selection may favor phenotypic variation, however its impact on the mechanistic underpinnings of phenotypic variation in M. longipes males is unknown. We therefore tested how genetic variation and phenotypic plasticity contribute to the maintenance of high variation in M. longipes male leg length. Artificially selected large and small male lines, generated through 15 sib-sib successive crosses from a natural population, showed a shifted distribution of male leg length towards the respective extreme phenotypes of the distribution (Figure 4A). The difference between these two lines held for both absolute and relative leg length, but the allometric coefficient remained, nonetheless, unchanged (Supplementary figure 5; Supplementary table 5). This shows that genotypic variation contributes to the variation in both rear leg length and body size.

Figure 4:
Figure 4:

Environmental and genetic contributions to rear leg length variation in males M. longipes. A) Rear leg length distributions of adult males from natural population (white) and from an inbred line that developed under poor (light grey) and rich (dark grey) conditions. B) Rear leg length distributions of adult males from natural population (white) and from two inbred lines that were selected for short (light grey) or long (dark grey) rear legs under rich condition. Normal curves were fitted to each distribution after testing for normality of each condition.

Next, we tested the reaction norm of one of these inbred lines in poor and rich nutritional condition. Despite near identical genotype, individuals reared in poor condition developed shorter legs than individuals reared in rich condition such that the distributions of the two treatments were almost non-overlapping (Figure 4B, Supplementary figure 6; Supplementary table 5). Importantly, this difference in leg length between the two treatments resulted mostly from differences in overall body size (t-test body length: t = 10.5643, df = 25.274, p-value = 9.244e-ll) but not in the scaling relationship as we failed to detect any significant difference in the allometric coefficient or the intercept between rich and poor conditions (Supplementary figure 6; Supplementary table 5). The same result was reached when we tested condition dependence in a laboratory population where no specific selection has been applied, although some statistical tests detected a small but significant difference in intercept between the two conditions (Supplementary figure 7; Supplementary table 5). This difference was nonetheless not significant when using a linear model (ANOVA, F(l,88)= 2.6202, p-value= 0.1076). We therefore conclude that, in M. longipes, male body size is highly condition-dependent but the rear legs are not or they are to a small extent after body size correction. Altogether, these results suggest that male leg length variation in nature results from the contribution of both genetic variation and strong condition dependence. The fluctuations in the amount of egg-laying floaters, combined with phenotypic plasticity, is expected to result in the maintenance of a certain degree of genetic variation in the population through the incomplete removal of alleles of small leg and body size. However, episodes of relaxed selection are not only known to increase genetic variation in the population, but also to favor the evolution of reaction norms and therefore increase phenotypic plasticity [40, 41].

Conclusions

This study provides a good example of how various ecological factors influence the intensity of sexual selection and ultimately the mechanisms and patterns of phenotypic variation. In the genus Microvelia, mating systems are diverse and are likely to influence the diversification of male-specific secondary sexual traits used in pre-mating copulatory strategies. The intense male competition to dominate egg-laying sites in M. longipes, unlike other Microvelia species, underlies the evolution of exaggerated leg length used as a weapon. Dominating males that intercept and copulate with gravid females on egg-laying sites gain a significant increase in their reproductive fitness by siring the majority of the eggs. This intense selection on increased leg length can, however, be relaxed when egg-laying sites are abundant thus allowing small males to fertilize a significant number of eggs. We have also shown that plasticity in response to nutritional condition along with genetic variation both contribute to the high phenotypic variation we observe in body and leg length. It is possible that fluctuating selection, combined with phenotypic plasticity, both facilitate the dramatic increase and maintenance of phenotypic variation in M. longipes compared to other Microvelia species. It is also important to note that the fluctuating selection described here (availability of egg-laying floaters) is independent of the individual condition. Therefore its influence on phenotypic variation cannot be the consequence of a pre-existing increase of condition-dependence, as it would be the case for fluctuating selection on food resources for example. Altogether, these results point to two ways in which alleles for small male body and leg size will be maintained in the population. First, because small males can sire a significant number of progeny due to possible episodes of relaxed selection. Second, because males with allelic combinations for low trait expression can develop larger body and leg size if they experience higher nutritional condition during development. Therefore condition dependence causes a non-linear relationship between genotypes and phenotypes, making directional selection less efficient in depleting genetic variation. In their opinion paper, Cornwallis and Uller [23] refer to this process as a “feedback loop between heterogeneity, selection and phenotypic plasticity”.

The findings outlined here open important research avenues to gain a general understanding of how sexual selection can impact phenotypic evolution. Microvelia longipes as a new hemimetabolous insect model with an exaggerated secondary sexual trait offers the opportunity to complete the substantial literature in holometabolous insects such as beetles or various flies [8, 42–45]. Males of many species of water striders employ water surface ripples as mating calls, and it is unknown whether females can deduce the size of the male from the ripple pattern and whether this would influence female choice [27, 46–49]. In addition, the number and the frequency of allelic variants underlying this trait and how they may interact with the environment remains to be tested. The ease of rearing and the relative short generation time make Microvelia longipes a powerful future model to study the extent to which genetic variation and environmental stimuli influence gene expression and ultimately phenotypic variation.

Author contributions

A.K. and W.T. designed research; W.T. performed research; A.K. and W.T. analyzed data; and A.K. and W.T. wrote the paper

Acknowledgements

We thank Emília Santos and Antonin Crumiére for help with collecting bugs, Felipe Moreira for help with species identification, Russell Bondurianski, Locke Rowe, Kevin Parsons, Gaël Yvert, François Leulier, Augustin Le Bouquin, Amélie Decaras, Cédric Finet, Aidamalia Vargas, Roberto Arbore for helpful discussions and comments on the manuscript, and David Armisén and Antoine Melet for help with genetic markers identification and data measurements. This work was supported by an ERC-CoG# 616346 and labex CEBA to AK, and a PhD fellowship from Ecole Doctorale BMIC de Lyon to W.T.

References

  1. 1.↵
    Darwin C. On the origin of species by means of natural selection, or, The preservation of favoured races in the struggle for life. London: J. Murray; 1859. ix, [1], 502, [1] fold, leaf of plates (32 at end advertisements) p.
    OpenUrl
  2. 2.↵
    Hall BHaBK. Variation: A Central Concept in Biology. Elsevier Academic Press ed2005.
  3. 3.↵
    1. Princeton, N.J.
    Andersson MB. Sexual selection. Princeton, N.J.: Princeton University Press; 1994. xx, 599 p. p.
    OpenUrlCrossRefPubMedWeb of Science
  4. 4.↵
    Darwin C. The descent of man, and selection in relation to sex. London,: J. Murray; 1871. 2 v. p.
  5. 5.↵
    McCullough EL, Ledger KJ, O’Brien DM, Emlen DJ. Variation in the allometry of exaggerated rhinoceros beetle horns. Anim Behav. 2015;109:133–40. doi: 10.1016/j.anbehav.2015.08.013. PubMed PMID: WOS:000363268300017.
    OpenUrlCrossRefPubMed
  6. 6.↵
    1. David M.
    2. Shuker LWS
    Emlen DJ. Reproductive contests and the evolution of extreme weaponry. In: David M. Shuker LWS, editor. The evolution of insect mating systems. Oxford University Press ed2014.
  7. 7.↵
    Zahavi A. Mate Selection - Selection for a Handicap. J Theor Biol. 1975;53(1):205–14. doi: Doi 10.1016/0022-5193(75)90111-3. PubMed PMID: WOS:A1975AR81900012.
    OpenUrlCrossRefPubMedWeb of Science
  8. 8.↵
    Emlen DJ, Warren IA, Johns A, Dworkin I, Lavine LC. A mechanism of extreme growth and reliable signaling in sexually selected ornaments and weapons. Science. 2012;337(6096):860–4. Epub 2012/07/28. doi: 10.1126/science.l224286. PubMed PMID: 22837386.
    OpenUrlAbstract/FREE Full Text
  9. 9.↵
    Rowe L, Houle D. The lek paradox and the capture of genetic variance by condition dependent traits. P R Soc B. 1996;263(1375):1415–21. doi: Doi 10.1098/rspb.1996.0207. PubMed PMID: WOS:A1996VQ62200022
    OpenUrlCrossRefPubMed
  10. 10.↵
    Andersson M. Female Choice Selects for Extreme Tail Length in a Widowbird. Nature. 1982;299(5886):818–20. doi: Doi 10.1038/299818a0. PubMed PMID: WOS:A1982PM85200043.
    OpenUrlCrossRefPubMed
  11. 11.↵
    Emlen DJ. The Evolution of Animal Weapons. Annu Rev Ecol Evol S. 2008;39:387–413. doi: 10.1146/annurev.ecolsys.39.110707.173502. PubMed PMID: WOS: 000261725500019.
    OpenUrlCrossRefPubMed
  12. 12.↵
    O’Brien DM, Katsuki M, Emlen DJ. Selection on an extreme weapon in the froglegged leaf beetle (Sagra femorata). Evolution. 2017;71(11):2584–98. doi: 10.1111/evo.13336. PubMed PMID: 28841226.
    OpenUrlCrossRefPubMed
  13. 13.
    1. Losos JB
    Miller CW. Sexual selection: Male-male competition. In: Losos JB, editor. The Princeton Guide to Evolution. Princeton: Princeton University Press ed2013.
  14. 14.↵
    Miller CW, Emlen DJ. Dynamic effects of oviposition site on offspring sexually-selected traits and scaling relationships. Evol Ecol. 2010;24(2):375–90. doi: 10.1007/s10682-009-9312-6. PubMed PMID: WOS:000274109600008.
    OpenUrlCrossRefPubMed
  15. 15.↵
    Kirkpatrick M, Ryan MJ. The Evolution of Mating Preferences and the Paradox of the Lek. Nature. 1991;350(6313):33–8. doi: Doi 10.1038/350033a0. PubMed PMID: WOS:A1991FA69300054.
    OpenUrlCrossRefPubMed
  16. 16.
    Fisher RA. The genetical theory of natural selection. Oxford,: The Clarendon Press; 1930. xiv, 272 p. p.
    OpenUrl
  17. 17.
    Houle D. Comparing Evolvability and Variability of Quantitative Traits. Genetics. 1992;130(1): 195–204. PubMed PMID: ISI:A1992GX54300018.
    OpenUrlAbstract/FREE Full Text
  18. 18.
    Radwan J. Maintenance of genetic variation in sexual ornaments: a review of the mechanisms. Genetica. 2008;134(1):113–27. doi: 10.1007/sl0709-007-9203-0. PubMed PMID: WOS:000258371900012.
    OpenUrlCrossRefPubMedWeb of Science
  19. 19.
    Pomiankowski A. Sexual Selection - the Handicap Principle Does Work Sometimes. Proc R Soc Ser B-Bio. 1987;231(1262):123–45. doi: Doi 10.1098/rspb. 1987.0038. PubMed PMID: WOS:A1987J032400008.
    OpenUrlCrossRefPubMed
  20. 20.
    Grafen A. Sexual Selection Unhandicapped by the Fisher Process. J Theor Biol. 1990;144(4):473–516 doi: Doi 10.1016/S0022-5193(05)80087-6. PubMed PMID: WOS:A1990DL42100003.
    OpenUrlCrossRefPubMedWeb of Science
  21. 21.↵
    Pomiankowski A, Moller AP. A Resolution of the Lek Paradox. P R Soc B. 1995;260(1357):21–9. doi: Doi 10.1098/rspb.l995.0054. PubMed PMID: WOS:A1995QX30200004.
    OpenUrlCrossRefPubMed
  22. 22.↵
    Miller CW, Svensson EL Sexual selection in complex environments. Annu Rev Entomol. 2014;59:427–45. doi: 10.1146/annurev-ento-011613-162044. PubMed PMID: 24160419.
    OpenUrlCrossRefPubMedWeb of Science
  23. 23.↵
    Cornwallis CK, Uller T. Towards an evolutionary ecology of sexual traits. Trends Ecol Evol. 2010;25(3):145–52. doi: 10.1016/j.tree.2009.09.008. PubMed PMID: 19853321.
    OpenUrlCrossRefPubMedWeb of Science
  24. 24.
    Robinson MR, Pilkington JG, Clutton-Brock TH, Pemberton JM, Kruuk LEB. Environmental heterogeneity generates fluctuating selection on a secondary sexual trait Curr Biol. 2008;18(10):751–7. doi: 10.1016/j.cub.2008.04.059. PubMed PMID: WOS: 000256047600028.
    OpenUrlCrossRefPubMed
  25. 25.
    Gosden TP, Svensson EL Spatial and temporal dynamics in a sexual selection mosaic. Evolution. 2008;62(4):845–56. doi: 10.1111/j.l558-5646.2008.00323.x. PubMed PMID: WOS:000254640900010.
    OpenUrlCrossRefPubMedWeb of Science
  26. 26.↵
    Johnston SE, Gratten J, Berenos C, Pilkington JG, Clutton-Brock TH, Pemberton JM, et al. Life history trade-offs at a single locus maintain sexually selected genetic variation. Nature. 2013;502(7469):93–+. doi: 10.1038/naturel2489. PubMed PMID: WOS: 00032 5106000037.
    OpenUrlCrossRefPubMedWeb of Science
  27. 27.↵
    Andersen NM. The semiaquatic bugs (Hemiptera: Gerromorpha). Klampenborg, Denmark.: Scandinavian Science Press LTD.; 1982.
  28. 28.↵
    Baker RH, Wilkinson GS. Phylogenetic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae). Evolution. 2001;55(7):1373–85. PubMed PMID: WOS:000170699300010.
    OpenUrlCrossRefPubMedWeb of Science
  29. 29.↵
    Arnqvist G, Rowe L. Sexual conflict. Princeton, N.J.: Princeton University Press; 2005. xii, 330 p. p.
    OpenUrlCrossRefPubMedWeb of Science
  30. 30.↵
    Da Motta FS, Moreira FFF, Crumiere AJJ, Santos ME, Khila A. A new species of Rhagovelia Mayr, 1865 (Hemiptera: Heteroptera: Veliidae) from French Guiana, with new records of Gerromorpha from the country. Zootaxa. 2018;4433(3):520–30. doi: 10.11646/zootaxa.4433.3.7. PubMed PMID: WOS:000435433900007.
    OpenUrlCrossRefPubMed
  31. 31.↵
    Taylor JS, McPherson EJ. Morphological Variation and Polyvoltinism of Microvelia pulchella (Heteroptera: Veliidae) in Southern Illinois, USA. Acta Societatiis Zoologicae Bohemicae. 1999.
  32. 32.↵
    Lanigan AC, Hyslop EJ. The aquatic and semiaquatic Hemiptera of Jamaica. J Freshwater Ecol. 2011;26(2):295–7. doi: 10.1080/02705060.2011.559335. PubMed PMID: WOS:000292949200016.
    OpenUrlCrossRefPubMed
  33. 33.↵
    Kokko H, Rankin DJ. Lonely hearts or sex in the city? Density-dependent effects in mating systems. Philos Trans R Soc Lond B Biol Sci. 2006;361(1466):319–34. doi: 10.1098/rstb.2005.1784. PubMed PMID: 16612890; PubMed Central PMCID: PMCPMC1569612.
    OpenUrlCrossRefPubMed
  34. 34.↵
    1. Shuker DM,
    2. Simmons LW
    Simmons LW. Sperm competition. In: Shuker DM, Simmons LW, editors. The evolution of insect mating systems. Oxford University Press ed2014.
  35. 35.↵
    Arnqvist G. Mate Guarding and Sperm Displacement in the Water Strider Gerris-Lateralis Schumm (Heteroptera, Gerridae). Freshwater Biol. 1988;19(2):269–74. doi: Doi 10.1111/j.1365-2427.1988.tb00347.x. PubMed PMID: WOS:A1988M736900011.
    OpenUrlCrossRefPubMed
  36. 36.
    Arnqvist G, Danielsson I. Copulatory behavior, genital morphology, and male fertilization success in water striders. Evolution. 1999;53(l):147–56. doi: Doi 10.2307/2640927. PubMed PMID: WOS:000078927800013.
    OpenUrlCrossRefPubMedWeb of Science
  37. 37.
    1. Crespi B
    Arnqvist G. The evolution of water strider mating systems: causes and consequences of sexual conflicts. In: Crespi B, editor. The Evolution of Mating Systems in Insects and Arachnids. Cambridge University Press ed1997.
  38. 38.↵
    Devost E, Turgeon J. The combined effects of pre- and post-copulatory processes are masking sexual conflict over mating rate in Gerris buenoi. J Evolution Biol. 2016;29(1): 167–77. doi: 10.1111/jeb.l2772. PubMed PMID: WOS:000368074900013.
    OpenUrlCrossRefPubMed
  39. 39.↵
    Simmons LW. Sperm Competition and Its Evolutionary Consequences in the Insects. Princeton University Press, Princeton, NJ ed 2001.
  40. 40.↵
    Hunt BG, Ometto L, Wurm Y, Shoemaker D, Yi SV, Keller L, et al. Relaxed selection is a precursor to the evolution of phenotypic plasticity. P Natl Acad Sci USA. 2011;108(38): 15936–41. doi: 10.1073/pnas.ll04825108. PubMed PMID: WOS:000295030000056.
    OpenUrlAbstract/FREE Full Text
  41. 41.↵
    Lahti DC, Johnson NA, Ajie BC, Otto SP, Hendry AP, Blumstein DT, et al. Relaxed selection in the wild. Trends Ecol Evol. 2009;24(9):487–96. doi: 10.1016/j.tree.2009.03.010. PubMed PMID: WOS:000270016800009.
    OpenUrlCrossRefPubMedWeb of Science
  42. 42.↵
    Toubiana W, Khila A. The benefits of expanding studies of trait exaggeration to hemimetabolous insects and beyond morphology. Curr Opin Genet Dev. 2016;39:14–20. doi: 10.1016/j.gde.2016.05.015. PubMed PMID: WOS:000388922900004.
    OpenUrlCrossRefPubMed
  43. 43.
    Moczek AP. Integrating micro- and macroevolution of development through the study of horned beetles. Heredity. 2006;97(3):168–78. Epub 2006/07/13. doi: 10.1038/sj.hdy.6800871. PubMed PMID: 16835592.
    OpenUrlCrossRefPubMedWeb of Science
  44. 44.
    Bonduriansky R. Condition dependence of developmental stability in the sexually dimorphic fly Telostylinus angusticollis (Diptera: Neriidae). J Evol Biol. 2009;22(4):861–72. Epub 2009/02/18. doi: JEB1686 [pii] 10.1111/j.1420-9101.2009.01686.x. PubMed PMID: 19220651.
    OpenUrlCrossRefPubMedWeb of Science
  45. 45.↵
    Chapman T, Pomiankowski A, Fowler K. Stalk-eyed flies. Curr Biol. 2005;15(14):R533–R5. doi: Doi 10.1016/j.cub.2005.07.015. PubMed PMID: WOS:000230903900006.
    OpenUrlCrossRefPubMed
  46. 46.↵
    Armisen D, Refki PN, Crumiere AJJ, Viala S, Toubiana W, Khila A. Predator strike shapes antipredator phenotype through new genetic interactions in water striders. Nature Communications. 2015;6. doi: Artn 8153 10.1038/Ncomms9153. PubMed PMID: WOS:000363016300002.
    OpenUrlCrossRefPubMed
  47. 47.
    Hayashi K. Alternative Mating Strategies in the Water Strider Gerris-Elongatus (Heteroptera, Gerridae). Behav Ecol Sociobiol. 1985;16(4):301–6. doi: Doi 10.1007/Bf00295542. PubMed PMID: WOS:A1985AHR1900002.
    OpenUrlCrossRefPubMed
  48. 48.
    Wilcox RS. Ripple Communication in Aquatic and Semiaquatic Insects. Ecoscience. 1995;2(2):109–15. doi: Doi 10.1080/11956860.1995.11682274. PubMed PMID: WOS:A1995TF50800001.
    OpenUrlCrossRefPubMed
  49. 49.↵
    Wilcox RS. Communication by Surface-Waves - Mating Behavior of a Water Strider (Gerridae). J Comp Physiol. 1972;80(3):255&. doi: Doi 10.1007/Bf00694840. PubMed PMID: WOS:A1972N753600003.
    OpenUrlCrossRefPubMed
  50. 50.↵
    Warton DI, Duursma RA, Falster DS, Taskinen S. smatr 3-an R package for estimation and inference about allometric lines. Methods Ecol Evol. 2012;3(2):257–9. doi: 10.1111/j.2041-210X.2011.00153.x. PubMed PMID: WOS:000302538500005.
    OpenUrlCrossRefPubMed
  51. 51.↵
    Crumiere AJJ, Santos ME, Semon M, Armisen D, Moreira FFF, Khila A. Diversity in Morphology and Locomotory Behavior Is Associated with Niche Expansion in the Semiaquatic Bugs. Curr Biol. 2016;26(24):3336–42. doi: 10.1016/j.cub.2016.09.061. PubMed PMID: WOS:000390666200027.
    OpenUrlCrossRefPubMed
  52. 52.↵
    Crumiere AJJ, Santos ME, Semon M, Armisen D, Moreira FFF, Khila A. Diversity in Morphology and Locomotory Behavior Is Associated with Niche Expansion in the Semiaquatic Bugs. Curr Biol. 2016;26(24):3336–42. PubMed PMID: Medline:27939311.
    OpenUrlCrossRefPubMed
  53. 53.↵
    Karaca M, Bilgen M, Onus AN, Ince AG, Elmasulu SY. Exact Tandem Repeats Analyzer (E-TRA): A new program for DNA sequence mining. J Genet. 2005;84(l):49–54. doi: Doi 10.1007/Bf02715889. PubMed PMID: WOS:000228875600008.
    OpenUrlCrossRefPubMed
  54. 54.↵
    Gloor GB, Preston CR, Johnsonschlitz DM, Nassif NA, Phillis RW, Benz WK, et al. Type-I Repressors of P-Element Mobility. Genetics. 1993;135(l):81–95. PubMed PMID: WOS:A1993LW03300009.
    OpenUrlAbstract/FREE Full Text
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Fluctuating selection strength and intense male competition underlie variation and exaggeration of a water strider’s male weapon
William Toubiana, Abderrahman Khila
bioRxiv 430314; doi: https://doi.org/10.1101/430314
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