Samuel Cotton

Do sexual ornaments demonstrate heightened condition-dependent expression as predicted by the handicap hypothesis?

The handicap hypothesis of sexual selection predicts that sexual ornaments have evolved heightened condition–dependent expression. The prediction has only recently been subject to experimental investigation. Many of the experiments are of limited value as they: (i) fail to compare condition dependence in sexual ornaments with suitable non–sexual trait controls; (ii) do not adequately account for body size variation; and (iii) typically consider no stress and extreme stress manipulations rather than a range of stresses similar to those experienced in nature. There is also a dearth of experimental studies investigating the genetic basis of condition dependence. Despite the common claim that sexual ornaments are condition–dependent, the unexpected conclusion from our literature review is that there is little support from well–designed experiments.

Sexual Selection and Condition-Dependent Mate Preferences

The last decade has witnessed considerable theoretical and empirical investigation of how male sexual ornaments evolve. This strong male-biased perspective has resulted in the relative neglect of variation in female mate preferences and its consequences for ornament evolution. As sexual selection is a co-evolutionary process between males and females, ignoring variation in females overlooks a key aspect of this process. Here, we review the empirical evidence that female mate preferences, like male ornaments, are condition dependent. We show accumulating support for the hypothesis that high quality females show the strongest mate preference. Nonetheless, this is still an infant field, and we highlight areas in need of more research, both theoretical and empirical. We also examine some of the wider implications of condition-dependent mating decisions and their effect on the strength of sexual selection.

CONDITION DEPENDENCE OF SEXUAL ORNAMENT SIZE AND VARIATION IN THE STALK-EYED FLY CYRTODIOPSIS DALMANNI (DIPTERA: DIOPSIDAE)

Abstract We used the stalk‐eyed fly Cyrtodiopsis dalmanni to examine predictions made by condition‐dependent handicap models of sexual selection. Condition was experimentally varied by manipulation of larval food availability. Cyrtodiopsis dalmanni is a highly dimorphic species exhibiting strong sexual selection, and the male sexual ornament (exaggerated eyespan) showed strong condition‐dependent expression relative to the homologous trait in females and nonsexual traits. Male eyespan also showed a great increase in standardized variance under stress, unlike nonsexual traits. The inflated variance of the male ornament was primarily attributable to condition‐dependent (but body‐size‐independent) increase in variance. Thus, evaluation of male eyespan allows females to gain additional information about male condition over and above that given by body size. These findings accord well with condition‐dependent handicap models of sexual selection.

Population consequences of environmental sex reversal.

When sex determination in a species is predominantly genetic but environmentally reversible, exposure to (anthropogenic) changes in the environment can lead to shifts in a populations sex ratio. Such scenarios may be common in many fishes and amphibians, yet their ramifications remain largely unexplored. We used a simple model to study the (short-term) population consequences of environmental sex reversal (ESR). We examined the effects on sex ratios, sex chromosome frequencies, and population growth and persistence after exposure to environmental forces with feminizing or masculinizing tendencies. When environmental feminization was strong, X chromosomes were driven to extinction. Analogously, extinction of normally male-linked genetic factors (e.g., Y chromosomes) was caused by continuous environmental masculinization. Although moderate feminization was beneficial for population growth in the absence of large viability effects, our results suggest that the consequences of ESR are generally negative in terms of population size and the persistence of sex chromosomes. Extreme sex ratios resulting from high rates of ESR also reduced effective population sizes considerably. This may limit any evolutionary response to the deleterious effects of ESR. Our findings suggest that ESR changes population growth and sex ratios in some counter-intuitive ways and can change the predominant factor in sex determination from genetic to fully environmental, often within only a few tens of generations. Populations that lose genetic sex determination may quickly go extinct if the environmental forces that cause sex reversal cease.

Variation in preference for a male ornament is positively associated with female eyespan in the stalk-eyed fly Diasemopsis meigenii.

There is currently much interest in mate preferences for sexual ornaments. However, few studies have focused on individual variation in mate preference despite its importance for the rate and direction of sexual selection. Females of the sexually dimorphic stalk-eyed fly, Diasemopsis meigenii, exhibit an unambiguous rejection response towards unattractive males bearing small ornaments. We investigated individual mate preferences using repeated sequential sampling of female rejection or acceptance responses to a wide range of male ornament phenotypes. We found significant variation in the strength of individual preference. In addition, preference was positively associated with female eyespan, a condition-dependent trait putatively linked to visual acuity.

Heightened condition dependence is not a general feature of male eyespan in stalk-eyed flies (Diptera: Diopsidae).

Stalk‐eyed flies are exemplars of sexual selection leading to the evolution of exaggerated male ornaments (eyespan). In Sphyracephala beccarri, there is no evidence for female mate choice for exaggerated male eyespan and only minor sex differences in eyespan. We used S. beccarri to test whether heightened condition dependence only evolves when male eyespan becomes sexually exaggerated. Male eyespan showed heightened condition dependence under food stress compared with a control trait (wing length). However, female eyespan displayed a similar pattern and there was no sex difference in the degree of increased eyespan sensitivity. The finding that eyespan is a sensitive indicator of food stress, even in an unexaggerated state, suggests that this may have acted as a pre‐adaptation to the role of eyespan in sexual signalling in other Diopsid species. These results are consistent with handicap theory and Fishers view of how sexual selection is initiated.

Eyespan reflects reproductive quality in wild stalk-eyed flies

Handicap models of sexual selection propose that females use male sexual ornaments as a cue in mate choice because they reflect commodities that increase female fitness, either directly or indirectly. In contrast to studies on vertebrates, most investigations of ornaments in insects and other invertebrate taxa have been conducted under laboratory conditions. There is a pressing need to address questions relating to sexual signalling of quality in natural populations, as the arbitrary and uniform environments found in the laboratory fail to reflect the world under which animals have evolved. We investigated associations between male ornaments (exaggerated eyespan), attractiveness, and reproductive quality in a wild population of the sexually ornamented stalk-eyed fly, Teleopsis dalmanni. We also explored the relationship between eyespan and reproductive quality in females to evaluate the potential for sexually antagonistic selection on eyespan. We show that eyespan is a generic correlate of reproductive quality, acting as a reliable mirror of variation in reproductive fitness in both sexes. Our findings suggest that male ornaments signal commodities that are of interest to females in the natural environment in which they, and mate preferences for them, have evolved. In addition, the covariance between female eyespan and reproductive output suggests that the former may be a reliable cue of quality in its own right. Our data provide important insights into the evolutionary forces that shape the evolution of exaggerated eyespan in wild populations of this species.

Male eyespan and resource ownership affect contest outcome in the stalk-eyed fly, Teleopsis dalmanni

The dominant theory for the evolution of male sexual ornaments is that they act as signals of male quality used by females in their mate choice. But these traits may also be used in male–male competition. In stalk-eyed flies, male eyespan (the distance between the eyes) is already known to play an important role in female mate choice. We investigated the influence of eyespan on male aggression over control of lek mating sites, both under controlled conditions and from field observations. Eyespan positively affected the number of aggressive encounters between two males on a lek. There were more aggressive interactions between large-eyespan males compared with small-eyespan males, and large-eyespan males won proportionately more aggressive interactions. Lek site ownership also influenced the outcome of aggression but to a smaller degree than eyespan. In addition, higher resource value, the number of females on a lek, increased the chance of aggression. The outcome of aggression between males is the control of lek aggregation sites, and this had direct consequences for male reproductive success, as lek owners gained more matings at both dusk and dawn. The importance of male–male competition in shaping sexual selection in stalk-eyed flies is discussed.

Highly variable sperm precedence in the stalk-eyed fly, Teleopsis dalmanni

BackgroundWhen females mate with different males, competition for fertilizations occurs after insemination. Such sperm competition is usually summarized at the level of the population or species by the parameter, P2, defined as the proportion of offspring sired by the second male in double mating trials. However, considerable variation in P2 may occur within populations, and such variation limits the utility of population-wide or species P2 estimates as descriptors of sperm usage. To fully understand the causes and consequences of sperm competition requires estimates of not only mean P2, but also intra-specific variation in P2. Here we investigate within-population quantitative variation in P2 using a controlled mating experiment and microsatellite profiling of progeny in the multiply mating stalk-eyed fly, Teleopsis dalmanni.ResultsWe genotyped 381 offspring from 22 dam-sire pair families at four microsatellite loci. The mean population-wide P2 value of 0.40 was not significantly different from that expected under random sperm mixing (i.e. P2 = 0.5). However, patterns of paternity were highly variable between individual families; almost half of families displayed extreme second male biases resulting in zero or complete paternity, whereas only about one third of families had P2 values of 0.5, the remainder had significant, but moderate, paternity skew.ConclusionOur data suggest that all modes of ejaculate competition, from extreme sperm precedence to complete sperm mixing, occur in T. dalmanni. Thus the population mean P2 value does not reflect the high underlying variance in familial P2. We discuss some of the potential causes and consequences of post-copulatory sexual selection in this important model species.

Comment: On the consequences of sexual selection for fisheries-induced evolution

It is becoming increasingly recognized that fishing (and other forms of nonrandom harvesting) can have profound evolutionary consequences for life history traits. A recent and welcome publication provided the first description of how sexual selection might influence the outcome of fisheries‐induced evolution (FIE). One of the main conclusions was that if sexual selection generates a positive relationship between body size and reproductive success, increased fishing pressure on large individuals causes stronger selection for smaller body size. Here, we re‐evaluate the sexual selection interpretation of the relationship between body size and reproductive success, and suggest it may in fact be representative of a more general case of pure natural selection. The consequences of sexual selection on FIE are likely to be complicated and dynamic, and we provide additional perspectives to these new and exciting results. Selection differentials and trait variance are considered, with density‐dependent and genetic effects on the strength and the direction of sexual selection given particular attention. We hope that our additional views on the role of sexual selection in FIE will encourage more theoretical and empirical work into this important application of evolutionary biology.