Runaway Selection Research Articles

Does Female Mate Choice Confer Direct Fitness Benefits? Results From a Tephritid Fruit Fly

The melon fly, Bactrocera cucurbitae (Coquillett), exhibits a lek mating system in which males aggregate on plants, weakly defend leaf territories that lack any resources vital to females, and produce pheromone to attract potential mates. Males are attracted to and feed on the plant-borne compound raspberry ketone (RK) as well as its synthetic analogue, cue lure (CL), and studies have demonstrated that females mate preferentially with males fed these chemicals over males denied them. The objective of the present study was to investigate whether females gained direct fitness benefits by mating with CL-fed males, potentially via CL-mediated modifications in male ejaculate composition and quantity that act to enhance female longevity and reproduction. Mating trials were first performed to re-confirm that CL-feeding conferred a mating advantage to males. Then, having detected an advantage, female survival, fecundity, and fertility were compared between females mated to CL-fed males versus nonfed males. In addition, the incidence and duration of successful egg-to-pupa development were compared between the two groups of females. None of the comparisons suggested that fitness was enhanced by mating with a CL-fed male, and one parameter—fertility or egg hatch rate—showed a potential cost to mating with CL-fed males. Thus, mating with CL-fed males does not appear to confer direct fitness benefits to females. Factors potentially confounding interpretation of this finding are noted, and the possible role of a runaway selection process, mediated via RK or CL consumption, in shaping female mate choice in this species is proposed.

How sexual selection can drive the evolution of costly sperm ornamentation.

Post-copulatory sexual selection (PSS), fuelled by female promiscuity, is credited with the rapid evolution of sperm quality traits across diverse taxa. Yet, our understanding of the adaptive significance of sperm ornaments and the cryptic female preferences driving their evolution is extremely limited. Here we review the evolutionary allometry of exaggerated sexual traits (for example, antlers, horns, tail feathers, mandibles and dewlaps), show that the giant sperm of some Drosophila species are possibly the most extreme ornaments in all of nature and demonstrate how their existence challenges theories explaining the intensity of sexual selection, mating-system evolution and the fundamental nature of sex differences. We also combine quantitative genetic analyses of interacting sex-specific traits in D. melanogaster with comparative analyses of the condition dependence of male and female reproductive potential across species with varying ornament size to reveal complex dynamics that may underlie sperm-length evolution. Our results suggest that producing few gigantic sperm evolved by (1) Fisherian runaway selection mediated by genetic correlations between sperm length, the female preference for long sperm and female mating frequency, and (2) longer sperm increasing the indirect benefits to females. Our results also suggest that the developmental integration of sperm quality and quantity renders post-copulatory sexual selection on ejaculates unlikely to treat male-male competition and female choice as discrete processes.

Male terrestrial salamanders demonstrate sequential mate choice based on female gravidity and size

In many vertebrate mating systems, mate choice evolves when signalling via visual, chemical or auditory traits is an energetically costly process. Selection may favour individuals that can discriminate among potential mates and invest in signalling to mates with particular characteristics. Most commonly, females with costly gametes are thought to be the more selective sex; however, runaway sexual selection can produce elaborate male ornaments and behaviours that are similarly costly to produce, which can lead to male mate choice. In this study, we used behavioural trials to experimentally test male mate choice in a terrestrial salamander, Plethodon shermani. We investigated whether males altered the proportion of time they spent performing a potentially costly courtship display, ‘foot dancing’, in the presence of females. Specifically, we explored male mate choice in two experiments: (1) measuring how males modified the time they invested in courtship based solely on female reproductive value, and (2) determining whether males varied the amount of time they invested in courting females of varying sizes but similar reproductive value. In the first experiment, we quantified the duration of male courtship displays when males were paired with females of differing levels of fecundity (nongravid, weakly gravid and strongly gravid). Males displayed longest for females of high reproductive value (strongly gravid females) and less for weakly gravid and nongravid females. In the second experiment, we showed that males paired sequentially with different-sized females of similar reproductive values displayed significantly more often to larger females (i.e. male effort positively correlated with female size). In conclusion, male P. shermani are one of the few vertebrates known to modify their display behaviour based on female mate quality, and visual signs, such as size, may provide honest indicators of fitness.

Social selection is a powerful explanation for prosociality.

Cultural group selection helps explain human cooperation, but social selection offers a complementary, more powerful explanation. Just as sexual selection shapes extreme traits that increase matings, social selection shapes extreme traits that make individuals preferred social partners. Self-interested partner choices create strong and possibly runaway selection for prosocial traits, without requiring group selection, kin selection, or reciprocity.

Coevolution of parasite virulence and host mating strategies

Parasites are thought to play an important role in sexual selection and the evolution of mating strategies, which in turn are likely to be critical to the transmission and therefore the evolution of parasites. Despite this clear interdependence we have little understanding of parasite-mediated sexual selection in the context of reciprocal parasite evolution. Here we develop a general coevolutionary model between host mate preference and the virulence of a sexually transmitted parasite. We show when the characteristics of both the host and parasite lead to coevolutionarily stable strategies or runaway selection, and when coevolutionary cycling between high and low levels of host mate choosiness and virulence is possible. A prominent argument against parasites being involved in sexual selection is that they should evolve to become less virulent when transmission depends on host mating success. The present study, however, demonstrates that coevolution can maintain stable host mate choosiness and parasite virulence or indeed coevolutionary cycling of both traits. We predict that choosiness should vary inversely with parasite virulence and that both relatively long and short life spans select against choosy behavior in the host. The model also reveals that hosts can evolve different behavioral responses from the same initial conditions, which highlights difficulties in using comparative analysis to detect parasite-mediated sexual selection. Taken as a whole, our results emphasize the importance of viewing parasite-mediated sexual selection in the context of coevolution.

Sexiness, Individual Condition, and Species Identity: The Information Signaled by Ornaments and Assessed by Choosing Females

Biologists have long debated the evolution of animal ornamentation via female choice. Much of the discussion of ornament evolution has focused on three hypotheses: the species recognition hypothesis, the indicator trait hypothesis, and the runaway sexual selection hypothesis. These models of sexual selection have generally been considered in isolation, with each assessed as a potential complete explanation for ornament evolution. In fact, any choosing female potentially benefits by assessing three distinct characteristics of a prospective mate—species identity, individual condition, and sexiness—such that there can be no comprehensive explanation of ornamentation without consideration of the need for females to assess these three key attributes of males. There is no logical basis for advocating for the importance of one of these classes of information over another. Consideration that all three assessments of prospective males work in tandem to shape the evolution of female preferences for male ornaments leads to a better understanding of the diversity of ornamentation within and among animal species.

A fish is not a fish: Patterns in fatty acid composition of aquatic food may have had implications for hominin evolution

From c. 2 Ma (millions of years ago) onwards, hominin brain size and cognition increased in an unprecedented fashion. The exploitation of high-quality food resources, notably from aquatic ecosystems, may have been a facilitator or driver of this phenomenon. The aim of this study is to contribute to the ongoing debate on the possible role of aquatic resources in hominin evolution by providing a more detailed nutritional context. So far, the debate has focused on the relative importance of terrestrial versus aquatic resources while no distinction has been made between different types of aquatic resources. Here we show that Indian Ocean reef fish and eastern African lake fish yield on average similarly high amounts of eicosapentaenoic acid (EPA), docosahexaenoic acid (DHA), and arachidonic acid (AA). Hence a shift from exploiting tropical marine to freshwater ecosystems (or vice versa) would entail no material difference in dietary long-chain polyunsaturated fatty acid (LC-PUFA) availability. However, a shift to marine ecosystems would likely mean a major increase in access to brain-selective micronutrients such as iodine. Fatty fish from marine temperate/cold waters yield twice as much DHA and four times as much EPA as tropical fish, demonstrating that a latitudinal shift in exploitation of African coastal ecosystems could constitute a significant difference in LC-PUFA availability with possible implications for brain development and functioning. We conclude that exploitation of aquatic food resources could have facilitated the initial moderate hominin brain increase as observed in fossils dated to c. 2 Ma, but not the exceptional brain increase in later stages of hominin evolution. We propose that the significant expansion in hominin brain size and cognition later on may have been aided by strong directional selecting forces such as runaway sexual selection of intelligence, and nutritionally supported by exploitation of high-quality food resources in stable and productive aquatic ecosystems.

The evolution of phenotypes and genetic parameters under preferential mating.

This article extends and adds more realism to Lande's analytical model for evolution under mate choice by using individual-based simulations in which females sample a finite number of males and the genetic architecture of the preference and preferred trait evolves. The simulations show that the equilibrium heritabilities of the preference and preferred trait and the genetic correlation between them (rG), depend critically on aspects of the mating system (the preference function, mode of mate choice, choosiness, and number of potential mates sampled), the presence or absence of natural selection on the preferred trait, and the initial genetic parameters. Under some parameter combinations, preferential mating increased the heritability of the preferred trait, providing a possible resolution for the lek paradox. The Kirkpatrick–Barton approximation for rG proved to be biased downward, but the realized genetic correlations were also low, generally <0.2. Such low values of rG indicate that coevolution of the preference and preferred trait is likely to be very slow and subject to significant stochastic variation. Lande's model accurately predicted the incidence of runaway selection in the simulations, except where preferences were relative and the preferred trait was subject to natural selection. In these cases, runaways were over- or underestimated, depending on the number of males sampled. We conclude that rapid coevolution of preferences and preferred traits is unlikely in natural populations, but that the parameter combinations most conducive to it are most likely to occur in lekking species.

Signal complexity and modular organization of the courtship behaviours of two sibling species of wolf spiders (Araneae: Lycosidae)

In this study, we compare the courtship behaviours of Pardosa proxima and P. vlijmi, two species of wolf spiders up to now regarded as “ethospecies”, by means of motion analysis methodologies. In particular, we investigate the features of the signals, aiming at understanding the evolution of the courtship and its role in species delimitation and speciation processes. In our model, we highlight a modular structure of the behaviours and the presence of recurring units and phases. According to other similar cases concerning animal communication, we observed one highly variable and one stereotyped phase for both species. The stereotyped phase is here regarded as a signal related to species identity or an honest signal linked directly to the quality of the signaler. On the contrary, the variable phase aims to facilitate signal detection and assessment by the female reducing choice costs or errors. Variable phases include cues arisen from Fisherian runaway selection, female sensory exploitation and remaining of past selections.

IDENTIFICATION OF GENETICALLY LINKED FEMALE PREFERENCE AND MALE TRAIT

Genetic variation in male traits and the female preferences for those traits allows for the evolution of sexual behavior. Trait-preference combinations are thought to improve the effectiveness of runaway sexual selection within a species, and are considered necessary for the induction of divergence between species. Novel traits, or variants of existing traits, and their associated preferences in the opposite sex are more likely to be maintained if they are genetically linked in proximity on a chromosome (the genetic coupling hypothesis), yet there is little empirical evidence that this genetic linkage occurs. Here we show for the first time that natural genetic variation at a single-linked region can induce both species-specific female choosiness and the male trait they are discriminating against. We found this effect in two separate regions of the genome, demonstrating that this linkage may be common. In contrast, female choosiness and male unattractiveness could not be alleviated by a single region. The close linkage of these loci and the strength of their effect provide an evolutionary means by which this preference-trait combination could arise and be maintained, thus enabling a more rapid route for runaway sexual selection, and providing empirical evidence supporting the genetic coupling hypothesis.

No evidence for rapid evolution of seed dispersal ability in range edge populations of the invasive species Senecio madagascariensis

AbstractTheory suggests that range edge populations of invading plants and animals may experience runaway selection for increased dispersal ability. This theory has been supported by field data for cane toads in Australia, and for Senecio inaequidens in Europe. In this study, we asked whether range edge populations of Senecio madagascariensis (Asteraceae), an invasive plant in eastern Australia, displayed higher dispersal ability that did populations from the established range. We measured 1363 diaspores from 33 populations. There was no significant difference in dispersal potential between populations from the range edge, and those from the established range (P = 0.19). We also used a glasshouse study to determine whether the range edge populations differed from populations in the established range in three critical life history traits: germination success, plant size and time to first reproduction. The only significant difference was for higher germination in range edge populations. The null result for dispersal ability is excellent news for land managers, as this is the first published evidence that selection for ever‐increasing dispersal rates is not ubiquitous in invading populations.

Evolution of lure response in tephritid fruit flies: phytochemicals as drivers of sexual selection

The males of many Bactrocera species (Diptera: Tephritidae) respond strongly and positively to a small number of plant-derived chemicals (= male lures). Males that have imbibed the lures commonly have a mating advantage over unfed males, but no female benefits have been demonstrated for females mating with lure-fed males. It has been hypothesized that the strong lure response is a case of runaway selection, where males receive direct benefits and females receive indirect benefits via ‘sexy sons’, or a case of sensory bias where females have a lower threshold response to lures. To test these hypotheses we studied the effects of lure feeding on male mating, remating and longevity; while for females that had mated with lure-fed males we recorded mating refractoriness, fecundity, egg viability and longevity. We used Bactrocera tryoni as our test animal and as lures the naturally occurring zingerone and chemically related, but synthetic chemical cuelure. Feeding on lures provided direct male benefits in greater mating success and increased multiple mating. For the first time, we recorded direct female effects: increased fecundity and reduced remating receptivity. Egg viability did not differ in females mated with lure-fed or unfed males. The life span of males and females exposed to lures was reduced. These results reveal direct, current-generation fitness benefits for both males and females, although the male benefits appear greater. We discuss that while lure response is indeed likely to be a sexual selection trait, there is no need to invoke runaway selection to explain its evolution.

Evolutionary suicide as a consequence of runaway selection for greater aggregation tendency

Aggregation of individuals is a common phenomenon in nature. By aggregating, individuals can reap benefits but may also be subject to associated costs from increased competition. The benefits of aggregation can depend on population density, which in turn can be affected by aggregation when it determines reproductive success of individuals. The Allee effect is often considered to be one of the factors that can explain the evolution of aggregation behavior. We investigated this hypothesis with a mathematical model which integrates population dynamics and evolution. Individuals gain synergistically from aggregation but suffer from scramble competition with aggregation tendency as an evolving trait. We found that aggregation behavior can stabilize the population dynamics and reduce population growth. The results show that the Allee effect alone is not sufficient for aggregative behavior to evolve as an evolutionarily stable strategy. We also found that weak local competition does not promote aggregation due to feedback from the population level: under low competition, the population can achieve high density such that aggregation becomes costly rather than beneficial. Our model instead exhibits an escalation of aggregation tendency, leading to the extinction of the population in a process known as evolutionary suicide. We conclude that for aggregation to evolve as an evolutionarily stable strategy we need to consider other factors such as inter-patch dispersal to new patches and avoidance of excessively large groups.

RUNAWAY SEXUAL SELECTION LEADS TO GOOD GENES

Mate choice and sexual displays are widespread in nature, but their evolutionary benefits remain controversial. Theory predicts these traits can be favored by runaway sexual selection, in which preference and display reinforce one another due to genetic correlation; or by good genes benefits, in which mate choice is advantageous because extreme displays indicate a well-adapted genotype. However, these hypotheses are not mutually exclusive, and the adaptive benefits underlying mate choice can themselves evolve. In particular, examining how and why sexual displays become indicators of good genes is challenging in natural systems. Here, we use experimental evolution in "digital organisms" to demonstrate the origins of condition-dependent indicator displays following their spread due to a runaway process. Surprisingly, handicap-like costs are not necessary for displays to become indicators of male viability. Instead, a pleiotropic genetic architecture underlies both displays and viability. Runaway sexual selection and good genes benefits should thus be viewed as interacting mechanisms that reinforce one another.

The evolution of optimal female mating rate changes the coevolutionary dynamics of female resistance and male persistence

Mating decisions usually involve conflict of interests between sexes. Accordingly, males benefit from increased number of matings, whereas costs of mating favour a lower mating rate for females. The resulting sexual conflict underlies the coevolution of male traits that affect male mating success ('persistence') and female traits that affect female mating patterns ('resistance'). Theoretical studies on the coevolutionary dynamics of male persistence and female resistance assumed that costs of mating and, consequently, the optimal female mating rate are evolutionarily constant. Costs of mating, however, are often caused by male 'persistence' traits that determine mating success. Here, we present a model where the magnitude of costs of mating depend on, and evolve with, male persistence. We find that allowing costs of mating to depend on male persistence results in qualitatively different coevolutionary dynamics. Specifically, we find that male traits such as penis spikes that harm females are not predicted to exhibit runaway selection with female resistance, in contrast to previous theory that predicts indefinite escalation. We argue that it is essential to determine when and to what extent costs of mating are caused by male persistence in order to understand and accurately predict coevolutionary dynamics of traits involved in mating decisions.

RUNAWAY SEXUAL SELECTION WITHOUT GENETIC CORRELATIONS: SOCIAL ENVIRONMENTS AND FLEXIBLE MATE CHOICE INITIATE AND ENHANCE THE FISHER PROCESS

Female mating preferences are often flexible, reflecting the social environment in which they are expressed. Associated indirect genetic effects (IGEs) can affect the rate and direction of evolutionary change, but sexual selection models do not capture these dynamics. We incorporate IGEs into quantitative genetic models to explore how variation in social environments and mate choice flexibility influence Fisherian sexual selection. The importance of IGEs is that runaway sexual selection can occur in the absence of a genetic correlation between male traits and female preferences. Social influences can facilitate the initiation of the runaway process and increase the rate of trait elaboration. Incorporating costs to choice do not alter the main findings. Our model provides testable predictions: (1) genetic covariances between male traits and female preferences may not exist, (2) social flexibility in female choice will be common in populations experiencing strong sexual selection, (3) variation in social environments should be associated with rapid sexual trait divergence, and (4) secondary sexual traits will be more elaborate than previously predicted. Allowing feedback from the social environment resolves discrepancies between theoretical predictions and empirical data, such as why indirect selection on female preferences, theoretically weak, might be sufficient for preferences to become elaborated.

Evolution of uncontrolled proliferation and the angiogenic switch in cancer

The major goal of evolutionary oncology is to explain how malignant traits evolve to become cancer ``hallmarks." One such hallmark---the angiogenic switch---is difficult to explain for the same reason altruism is difficult to explain. An angiogenic clone is vulnerable to ``cheater" lineages that shunt energy from angiogenesis to proliferation, allowing the cheater to outcompete cooperative phenotypes in the environment built by the cooperators. Here we show that cell- or clone-level selection is sufficient to explain the angiogenic switch, but not because of direct selection on angiogenesis factor secretion---angiogenic potential evolves only as a pleiotropic afterthought. We study a multiscale mathematical model that includes an energy management system in an evolving angiogenic tumor. The energy management model makes the counterintuitive prediction that ATP concentration in resting cells increases with increasing ATP hydrolysis, as seen in other theoretical and empirical studies. As a result, increasing ATP hydrolysis for angiogenesis can increase proliferative potential, which is the trait directly under selection. Intriguingly, this energy dynamic allows an evolutionary stable angiogenesis strategy, but this strategy is an evolutionary repeller, leading to runaway selection for extreme vascular hypo- or hyperplasia. The former case yields a tumor-on-a-tumor, or hypertumor, as predicted in other studies, and the latter case may explain vascular hyperplasia evident in certain tumor types.

So Small, So Loud: Extremely High Sound Pressure Level from a Pygmy Aquatic Insect (Corixidae, Micronectinae)

To communicate at long range, animals have to produce intense but intelligible signals. This task might be difficult to achieve due to mechanical constraints, in particular relating to body size. Whilst the acoustic behaviour of large marine and terrestrial animals has been thoroughly studied, very little is known about the sound produced by small arthropods living in freshwater habitats. Here we analyse for the first time the calling song produced by the male of a small insect, the water boatman Micronecta scholtzi. The song is made of three distinct parts differing in their temporal and amplitude parameters, but not in their frequency content. Sound is produced at 78.9 (63.6–82.2) SPL rms re 2.10−5 Pa with a peak at 99.2 (85.7–104.6) SPL re 2.10−5 Pa estimated at a distance of one metre. This energy output is significant considering the small size of the insect. When scaled to body length and compared to 227 other acoustic species, the acoustic energy produced by M. scholtzi appears as an extreme value, outperforming marine and terrestrial mammal vocalisations. Such an extreme display may be interpreted as an exaggerated secondary sexual trait resulting from a runaway sexual selection without predation pressure.

Runaway cultural niche construction.

Cultural niche construction is a uniquely potent source of selection on human populations, and a major cause of recent human evolution. Previous theoretical analyses have not, however, explored the local effects of cultural niche construction. Here, we use spatially explicit coevolutionary models to investigate how cultural processes could drive selection on human genes by modifying local resources. We show that cultural learning, expressed in local niche construction, can trigger a process with dynamics that resemble runaway sexual selection. Under a broad range of conditions, cultural niche-constructing practices generate selection for gene-based traits and hitchhike to fixation through the build up of statistical associations between practice and trait. This process can occur even when the cultural practice is costly, or is subject to counteracting transmission biases, or the genetic trait is selected against. Under some conditions a secondary hitchhiking occurs, through which genetic variants that enhance the capability for cultural learning are also favoured by similar dynamics. We suggest that runaway cultural niche construction could have played an important role in human evolution, helping to explain why humans are simultaneously the species with the largest relative brain size, the most potent capacity for niche construction and the greatest reliance on culture.

Evolution of Nutrient Uptake Reveals a Trade‐Off in the Ecological Stoichiometry of Plant‐Herbivore Interactions

Nutrient limitation determines the primary production and species composition of many ecosystems. Here we apply an adaptive dynamics approach to investigate evolution of the ecological stoichiometry of primary producers and its implications for plant-herbivore interactions. The model predicts a trade-off between the competitive ability and grazing susceptibility of primary producers, driven by changes in their nutrient uptake rates. High nutrient uptake rates enhance the competitiveness of primary producers but also increase their nutritional quality for herbivores. This trade-off enables coexistence of nutrient exploiters and grazing avoiders. If herbivores are not selective, evolution favors runaway selection toward high nutrient uptake rates of the primary producers. However, if herbivores select nutritious food, the model predicts an evolutionarily stable strategy with lower nutrient uptake rates. When the model is parameterized for phytoplankton and zooplankton, the evolutionary dynamics result in plant-herbivore oscillations at ecological timescales, especially in environments with high nutrient availability and low selectivity of the herbivores. High herbivore selectivity stabilizes the community dynamics. These model predictions show that evolution permits nonequilibrium dynamics in plant-herbivore communities and shed new light on the evolutionary forces that shape the ecological stoichiometry of primary producers.