Asymmetric dominance and asymmetric mate choice oppose premating isolation after allopatric divergence

Assortative mating promotes reproductive isolation and allows allopatric speciation processes to continue in secondary contact. As mating patterns are determined by mate preferences and intrasexual competition, we investigated male–male competition and behavioral isolation in simulated secondary contact among allopatric populations. Three allopatric color morphs of the cichlid fish Tropheus were tested against each other. Dyadic male–male contests revealed dominance of red males over bluish and yellow‐blotch males. Reproductive isolation in the presence of male–male competition was assessed from genetic parentage in experimental ponds and was highly asymmetric among pairs of color morphs. Red females mated only with red males, whereas the other females performed variable degrees of heteromorphic mating. Discrepancies between mating patterns in ponds and female preferences in a competition‐free, two‐way choice paradigm suggested that the dominance of red males interfered with positive assortative mating of females of the subordinate morphs and provoked asymmetric hybridization. Between the nonred morphs, a significant excess of negative assortative mating by yellow‐blotch females with bluish males did not coincide with asymmetric dominance among males. Hence, both negative assortative mating preferences and interference of male–male competition with positive assortative preferences forestall premating isolation, the latter especially in environments unsupportive of competition‐driven spatial segregation.     

Asynchronous arrival pattern, operational sex ratio and occurrence of multiple paternities in a territorial breeding anuran, Rana dalmatina

Understanding why females mate multiply is a major issue in evolutionary ecology. We investigated the consequences of an asynchronous arrival pattern on male competition and multiple paternity in the apparently monoandrous agile frog ( Rana dalmatina ). The largest frogs arrived first and both males and females lost weight significantly during the spawning period. Asynchronous arrival at breeding sites resulted in a male-biased operational sex ratio (OSR). The OSR was more strongly male-biased at the beginning and at the end of the breeding period when the number of satellite males increased. All females mated only once, but multiple paternity within clutches occurred at the beginning and the end of the breeding period. The influence of asynchronous arrival and biased sex ratio suggests that reduced variance or bet-hedging promoting female fitness had only a reduced role in the evolution of polyandry, and polyandry is likely to be associated with male benefits. Polyandry in frogs can be explained either by forced mating as a result of sexual conflict or by clutch piracy. By modifying intrasexual competition, asynchronous arrival and changes in OSR may have a decisive influence upon the evolution of mating systems and favour both polyandry and stable coexistence of alternative mating behaviour.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 86 , 191–200.     

Polyandry in Bicyclus anynana Butterflies Results from Sexual Conflict over Mating

Although only one or just a few matings are considered sufficient to maximise a female's reproductive success, polyandry is a common mating system in insects and other animals. Female polyandry may either result from direct or indirect benefits of mating multiply, or from male harassment and thus sexual conflict over mating. Here, we test whether the latter is involved in determining female mating frequency in the butterfly Bicyclus anynana. We used a full‐factorial design with three different sex ratios and densities each, resulting in a total of nine treatment groups. Sex ratio but not density affected female mating frequency, which increased with an increasingly male‐biased sex ratio. Our results thus suggest that female polyandry in B. anynana results from sexual conflict, although females seem to be able to reject courting males at least to some extent. Therefore, polyandry in this species may occur in the first place from convenience, as the costs of resisting male harassment may be higher than mating repeatedly.     

Male breeding behaviour and mate acquisition in the Common toad, Bufo bufo

The breeding behaviour of a Common toad ( Bufo bufo ) population was studied at a breeding pond on Portland, Dorset. Major toad movements towards the breeding pond occurred on warm, wet nights when the temperature did not fall below 6°C. Males arrived earlier than females resulting in an initially exaggerated sex ratio which then slowly reduced as the breeding season progressed. No size assortative pairing was found although large males were more successful at mating than small males. Although males demonstrated no ESS (evolutionary stable strategy) in searching for a female between sites within the pond evidence suggesting the existence of one between the pond and an undefined area surrounding it was found.     

On the role of sexual selection in ecological divergence: a test of body‐size assortative mating in the eastern newt Notophthalmus viridescens

Speciation processes initiated by divergent selection often fail to complete; yet, how sexual selection is involved in the progress of ecological speciation is rarely understood. Intraspecific body‐size variation affects mate preference and male–male competition, which can consequently lead to assortative mating based on body size. In the present study, we tested the importance of body size difference in the potential of assortative mating between the two eastern newt subspecies, larger Notophthalmus viridescens viridescens and smaller Notophthalmus viridescens dorsalis. Through differential expression of life‐cycle polyphenism, these two subspecies are adapted to contrasting environments, which has likely led to the subspecific body‐size difference. We found that males of both subspecies preferred larger females of N. v. viridescens as mates presumably because of the fecundity advantage of larger females. On the other hand, no evidence of female choice was found. Larger males of N. v. viridescens exhibited greater competitive ability and gained primary access to larger females of their own kind. However, smaller males were able to overcome their inferior competitive ability by interfering with larger males' spermatophore transfer and sneakily mating with larger females. Thus, the subspecific body‐size difference importantly affected sexual selection processes, resulting in nonrandom but not completely assortative mating patterns between the larger and smaller subspecies. Although life‐cycle polyphenism facilitates the intraspecific ecological divergence within N. v. viridescens sexual selection processes, namely smaller males' mate preference for larger females and sexual interference during spermatophore transfer, may be halting completion of the ecological speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 884–897.     

Impact of male alternative reproductive tactics on female costs of sexual conflict under variation in operational sex ratio and population density

Sexual conflict over mating rate is both pervasive and evolutionarily costly. For females, the lifetime reproductive fitness costs that arise through interactions with potential mates will be influenced by the frequency of such interactions, and the fitness cost of each interaction. Both of these factors are likely to be influenced by variation in operational sex ratio (OSR) and population density. Variation in OSR‐ and density‐dependent male alternative reproductive tactics (ARTs) may be particularly important if the fitness costs that females experience vary with the reproductive tactics that males express. Using a simple model, we consider several examples of OSR‐ and/or density‐dependent variation in male ARTs and the frequency of male–female interactions, and find that variation in the expression of male ARTs has the potential to augment or diminish the costs of frequent male interactions for females. Accurately documenting variation in the expression of male ARTs and associated female fitness costs will benefit future work in this area.     

Divergent host plant preference causes assortative mating between sympatric host races of the ladybird beetle,Henosepilachna diekei

Divergent host preference (i.e. host fidelity) plays a significant role in the speciation process in phytophagous insects. However, how and to what extent this divergence reduces gene flow between populations has rarely been measured. Here, we estimated the intensity of assortative mating caused solely by host fidelity in two host races of the phytophagous ladybird beetle Henosepilachna diekei, specialized on Mikania micrantha (Asteraceae) and Leucas lavandulifolia (Lamiaceae) in West Java, Indonesia. These host races mated randomly in the absence of host plants under laboratory conditions, but demonstrated nearly complete assortative mating in field cages with the two host plants, by spending almost all of their time on their respective host plants. The frequency of assortative mating in the field cages was not affected drastically by host plant patch structure. These results suggest that fidelity to the different host plants yields directly almost complete reproductive isolation between the host races by limiting the habitat on the respective host plant. In addition, the high host fidelity also ensures female oviposition on the original host plant. As larvae cannot survive on non‐host plants, a positive association between female oviposition preference and larval performance on the host plant on which the beetles are specialized will further facilitate the evolution of host fidelity. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 606–614.     

Male‐mimicking females increase male‐male interactions,and decrease male survival and condition in a female‐polymorphic damselfly

Biologists are still discovering diverse and powerful ways sexual conflicts shape biodiversity. The present study examines how the proportion of females in a population that exhibit male mimicry, a mating resistance trait, influences conspecific males’ behavior, condition, and survival. Like most female‐polymorphic damselflies, Ischnura ramburii harbors both “andromorph” females, which closely resemble males, and sexually dimorphic “gynomorph” counterparts. There is evidence that male mimicry helps andromorphs evade detection and harassment, but males can also learn to target locally prevalent morph(s) via prior mate encounters. I hypothesized that the presence of male mimics could therefore predispose males to mate recognition errors, and thereby increase rates of costly male‐male interactions. Consistent with this hypothesis, male‐male interaction rates were highest in mesocosms containing more andromorph (vs. gynomorph) females. Males in andromorph‐biased mesocosms also had lower final body mass and higher mortality than males assigned to gynomorph‐majority treatments. Male survival and body mass were each negatively affected by mesocosm density, and mortality data revealed a marginally significant interaction between andromorph frequency and population density. These findings suggest that, under sufficiently crowded conditions, female mating resistance traits such as male mimicry could have pronounced indirect effects on male behavior, condition, and survival.     

Mating pattern variability among western toad (Bufo boreas) populations

Summary Breeding ecology and mating patterns of the western toad, Bufo boreas, were examined in three large explosively breeding populations in the Oregon Cascade Mountains. Two mating patterns occurred variably within and among the three populations. First, a large male mating advantage was observed in two of the three populations when data from all the days of data collection were combined. When each day of breeding was analyzed separately, there was a large male mating advantage on 3 of 5 days at one population, and mating was random on all days at the two other populations. The second mating pattern, positive assortative mating by size, was observed at two of the three populations. This pattern was found on separate days of breeding as well as when data from all days were combined at one population, and on only one day of breeding at the second population.In a survey of anuran amphibian mating patterns, intraspecific variation was found in 13 of 15 species, including the present study of the western toad. Intrapopulation variation in mating patterns among breeding years has been observed in 5 of 8 anurans, whereas within-site, within-year mating pattern variation has only been reported for the western toad. These results strongly suggest that anuran mating patterns are frequently neither species-specific nor population-specific attributes. Variable mating patterns were most commonly observed in explosively-breeding anurans. Explosive breeders may be susceptible to variable mating patterns because they may be more sensitive to fluctuations in environmental conditions, demographic parameters, and the intensities of intrasexual competition and mate choice.     

Is size assortative mating in Paracalliope fluviatilis (Crustacea: Amphipoda) explained by male–male competition or female choice?

Field and laboratory studies were used to assess: (1) whether size assortative mating occurred in the New Zealand amphipod Paracalliope fluviatilis and (2) hypotheses developed to explain size assortative mating. We found that assortative mating occurred and that larger females carried more eggs, suggesting they may be more valuable as mates. Laboratory experiments were then used to determine whether: (1) male size influenced the size of the female selected (mechanical constraints hypothesis); (2) male size influenced pairing success in the presence of competition (intrasexual selection hypothesis); (3) take‐overs of females occurred and whether large males were more successful (intrasexual selection hypothesis); (4) guard duration varied relative to male and female size (guard duration hypothesis); and (5) females had control over pairing success and guard duration (intersexual selection hypothesis). Although there was evidence to suggest the existence of intrasexual competition for mates (i.e. both small and large males preferred large females), there was no evidence of overt competition (i.e. takeovers of paired females). There was also no difference with respect to how long small and large males guarded females, but large females were guarded longer by both male size classes. Females handicapped by having their mobility reduced were guarded for the same duration as control females but males were more likely to pair with handicapped females, suggesting that they were easier to amplex. Given the lack of evidence for direct male–male competition or female choice, we suggest that assortative mating may be the result of: (1) indirect competition (e.g. in situ large males may be better able to access and amplex the largest females) or (2) female resistance to small males in combination with higher costs that small males may incur in securing large females. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 92 , 173–181.     

Extreme Promiscuity in a Mating System Dominated by Sexual Conflict

Coelopids live in wrack beds consisting of seaweed washed up on beaches. Their mating system is characterized by sexual conflict and convenience polyandry, with females resisting male mating attempts. We estimated the level of harassment by males and the success rate of rejection by females collected from a high density wild population. Males mounted a female every 8.41 min. Of these mounts 35% resulted in copulation. This suggests that females could be mated up to 5 times every 2 h. Females typically live for 3 weeks, and thus, could mate with hundreds of males during their lifetime. We found a 50:50 sex ratio throughout the wrack bed revealing that females do not avoid male harassment by leaving the wrack bed when not ovipositing.     

An empirical demonstration of the ideal free distribution: Little Grebes Tachybaptus ruficollis breeding in intensive agricultural landscapes

The ideal free distribution (IFD) model predicts that a density‐dependent mechanism operates to regulate habitat selection and reproductive performance. We studied a Little Grebe Tachybaptus ruficollis population, which breeds on irrigation ponds in the Vega Baja Valley (southeastern Spain) to test the premises of the IFD model. These ponds are highly dynamic because they are managed according to agricultural requirements, and are subject to different levels of disturbance, which can change the quality of individual ponds across the landscape. Surveys were carried out during the breeding season from 2002 to 2006, with reproduction performance estimated during two consecutive breeding seasons, 2003 and 2004. Occupation frequency differed from random, indicating preference for some ponds over others. Habitat features such as pond construction and design, the presence of submerged vegetation, vegetation along the shore and reed beds, and pond area correlated with occupation frequency and might be considered to be indicators of pond quality. Ponds were occupied sequentially from best to worst. Thus, when the population size increased, the number of low‐quality ponds occupied also increased. High‐quality ponds held more breeding pairs than low‐quality ones, resulting in the mean reproductive success per breeding pair being independent of pond quality. Little Grebes therefore occupy ponds in a manner consistent with the expectations of the IFD model.     

Operational sex ratio,reproductive costs,and the potential for intrasexual competition

Even though numerous metrics exist, we still appear to be far from a consensual view on the best way of measuring or predicting the potential strength of sexual selection. One of the earliest and simplest metrics devised was the operational sex ratio (OSR) (i.e. the ratio between sexually active males and females in a population), and even, if heavily criticized, the OSR can still be viewed as a valuable measure of the potential levels of intrasexual competition. Because this ratio is influenced by the time that individuals spend in the mating pool, the OSR depends on our ability to determine who is indeed ready to mate. Moreover, because the proximate effects of OSR on mate monopolization might not be immediately apparent, we should be prepared to account for its association with the conditions making selection favour traits that reduce the time needed to acquire additional mating opportunities. Using the worm pipefish as a working model, we conducted a more stringent calculation of the OSR by eliminating individuals that, although present, do not appear to be able to reproduce, as determined by an analysis of female size classes with immature or spent ovaries and male classes without pregnancy events. Accordingly, the OSR was not only capable of correctly highlighting the potential for intrasexual competition, but also was able to translate the desertion of individuals from the mating pool as the breeding season progressed into meaningful correlations with variables associated with reproductive investment and costs (i.e. gonad investment and energy reserves). As demonstrated, the predictive power of the OSR can be broader than anticipated, depending primarily on our ability to effectively discriminate which individuals are indeed ready to mate. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 477–484.     

Mechanisms of reinforcement in natural and simulated polymorphic populations

Reinforcement speciation is the process whereby selection against hybrids drives the evolution of enhanced pre‐mating reproductive isolation. Work has focused on divergent mating preferences (assortative mating) but pre‐mating isolation can also arise via various migration modification behaviours, such as divergent habitat preferences. The relative importance of these two different mechanisms of reinforcement remains unclear. A recent theoretical model (Yukilevich–True model) found that relative fixation probabilities between these mechanisms can vary. Additionally, natural populations of Timema cristinae walking‐sticks exhibit variation (polymorphism) in both mechanisms, generating questions about the patterns expected for allele frequencies prior to fixation, during the early stages of the speciation process. In the present study, we report: (1) new analyses examining the correlation between fixation probabilities for assortative mating and migration modification in the Yukilevich–True model; (2) novel simulations examining allele frequencies in polymorphic populations; and (3) empirical patterns of reinforcement in T. cristinae in the context of theoretical predictions. Simulations of both types yielded congruent results, revealing that the outcome of reinforcement was dependent on the strength of selection. Under weak selection, reinforcement by either mechanism is unlikely. Under intermediate selection, the conditions favoring the rise and fixation of one mechanism favored the rise and fixation of the other. However, assortative mating evolved somewhat more readily than migration modification. Populations of T. cristinae, which experience such intermediate selection, supported these predictions. Under strong selection, the evolution of migration modification generally interfered with the evolution of assortative mating by decreasing migration between populations, thereby reducing selection for assortative mating. Congruence of the results for allele frequencies versus fixation probabilities suggests that similar patterns of reinforcement are expected during different stages of the speciation process. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 305–319.     

OPERATIONAL SEX RATIO BUT NOT DENSITY AFFECTS SEXUAL SELECTION IN A FISH

The operational sex ratio (OSR) and density are considered important factors affecting the strength of sexual selection. Although there is increasing evidence that OSR and density affect the potential for sexual selection, few studies have addressed whether this is realized in phenotypic selection and how the two factors interact. We manipulated OSR (three levels) and male density (two levels) in 36 experimental breeding populations of Gobiusculus flavescens—a fish with paternal care. We measured mating competition behavior, the opportunity for selection (I), and selection on four morphological traits in males. We found sexual selection on two male traits, with the strongest selection being 20% of I. As predicted from OSR theory, increasing female scarcity caused males to become more competitive, concomitant with an increase in I and selection on morphological traits. Model simulations of I based on random mating (I_min) and maximum mate monopolization (I_max) demonstrated that the potential for sexual selection was close to its theoretical maximum across the range of OSRs. However, male density and its interaction with the OSR did not affect sexual selection. We argue that a multifaceted approach, combining mating behavior and selection analyses, can help us to understand how ecological factors affect sexual selection.     

Mating Patterns of Red-Eyed Treefrogs, Agalychnis callidryas and A. moreletii

Deviations from random mating in frogs are often explained by two different size‐based patterns. The large‐male mating advantage predicts that males found in amplexus with females will be larger on average than non‐amplectant males, whereas size‐assortative mating predicts that males and females found in amplexus will maintain an optimal size ratio. Both these pairing patterns are consistent with a female mating preference for larger males, or for males of a given size relative to the choosy female. I examined pairing patterns of two species of Neotropical hylids, Agalychnis callidryas and A. moreletii for three consecutive breeding seasons in Belize, Central America to evaluate whether mating behavior was influenced by either a large‐male mating advantage or size‐assortative mating. For each species, I compared size traits between amplectant and non‐amplectant males, and within amplectant pairs, and I quantified fertilization success for each amplectant pair. For both species I found evidence of deviations from random mating by size, but the nature of the deviations varied between species and among years. The proportion of eggs fertilized was consistently high among years for both species and there was no relationship between fertilization success and the size ratio of amplectant pairs. These data are consistent with female mate preference, but a role for male–male competition cannot be excluded. My findings suggest that mating patterns may be density‐dependent and that the nature and intensity of sexual selection may be increased by extreme environmental conditions.     

Size-related mating and mate guarding in the orb-web spiderNephila clavata (Araneae,Araneidae)

The orb-web spiderNephila clavata satisfies three conditions for assortative mating proposed by Ridley (The Explanation of Organic Diversity. The Comparative Method and Adaptations for Mating, Clarendon, Oxford, 1983); (1) a large male advantage in male-male competition, (2) a correlation between female size and fecundity, and (3) a long pairing duration. To test Ridley's hypothesis, size assortative mating and guarding were examined in the field. When data were pooled over time, assortative mating was found but this was due to temporal covariation of body sizes of males and receptive females. After controlling for the effect of time, size assortative guarding was not detected, although females guarded by males were larger than those not guarded in the early breeding season. Possible reasons for the absence of size assortative guarding were discussed.     

Revealing the mechanisms of sexual isolation in a case of sympatric and parallel ecological divergence

Two ecotypes of a marine intertidal snail (Littorina saxatilis), living at different microhabitats and shore levels, have evolved in sympatry and in parallel across the Galician rocky shore. These ecotypes differ in many traits (including size) due to differential adaptation. They meet, mate assortatively, and partially hybridize at the mid shore where the two microhabitats overlap. The partial sexual isolation observed is claimed to be a side‐effect of the size differences between ecotypes combined with a size assortative mating found in most populations of this species. We investigated this hypothesis using three complementary experimental approaches. First, we investigated which of the different shell variables contributed most to the variation in individual sexual isolation in the field by using two new statistics developed for that purpose: (1) pair sexual isolation and (2) r_i, which is based on the Pearson correlation coefficient. We found that size is the most important trait explaining the sexual isolation and, in particular, the males appear to be the key sex contributing to sexual isolation. Second, we compared the size assortative mating between regions: exposed rocky shore populations from north‐westwern Spain (showing incomplete reproductive isolation due to size assortative mating) and protected Spanish and Swedish populations (showing size assortative mating but not reproductive isolation between ecomorphs). Most of the variation in size assortative mating between localities was significantly explained by the within‐population level of variation on size. Third, we performed a laboratory male choice experiment, which further suggested that the choice is made predominantly on the basis of size. These results confirm the mechanism proposed to explain the sexual isolation in the Galician hybrid zone and thus support this case as a putative example of parallel incipient speciation. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94 , 513–526.     

Patterns of synchrony in natterjack toad breeding activity and reproductive success at local and regional scales

Empirical studies of the spatiotemporal dynamics of populations are required to better understand natural fluctuations in abundance and reproductive success, and to better target conservation and monitoring programmes. In particular, spatial synchrony in amphibian populations remains little studied. We used data from a comprehensive three year study of natterjack toad Bufo calamita populations breeding at 36 ponds to assess whether there was spatial synchrony in the toad breeding activity (start and length of breeding season, total number of egg strings) and reproductive success (premetamorphic survival and production of metamorphs). We defined a novel approach to assess the importance of short‐term synchrony at both local and regional scales. The approach employs similarity indices and quantifies the interaction between the temporal and spatial components of populations using mixed effects models. There was no synchrony in the toad breeding activity and reproductive success at the local scale, suggesting that populations function as individual clusters independent of each other. Regional synchrony was apparent in the commencement and duration of the breeding season and in the number of egg strings laid (indicative of female population size). Regional synchrony in both rainfall and temperature are likely to explain the patterns observed (e.g. Moran effect). There was no evidence supporting regional synchrony in reproductive success, most likely due to spatial variability in the environmental conditions at the breeding ponds, and to differences in local population fitness (e.g. fecundity). The small scale asynchronous dynamics and regional synchronous dynamics in the number of breeding females indicate that it is best to monitor several populations within a subset of regions. Importantly, variations in the toad breeding activity and reproductive success are not synchronous, and it is thus important to consider them both when assessing the conservation status of pond‐breeding amphibians.     

Cost of sexually embracing a large female offset by the number of eggs fertilized for small male Bufo bufo L.

When pairing with high quality females, a male increases its fitness through an increased number and/or quality of sired offsprings. In anurans, size has often been used as a measure of female quality. In the present study, we examined the effects of pairing with large females for small males in the common toad, Bufo bufo . For the first time in anurans, we show a fitness cost for males to maintain amplexus with a large female. Indeed, although we did not detect any effect of male size on male pairing success in a first breeding event in the presence of other competing males, when males that were successful in the first breeding event were tested for a second time, male pairing success strongly decreased when they had been first paired with a large female. However, the higher fecundity of large females (1.52-fold more than that of small females) may override this pairing cost, especially because high fertilization rate was not linked to male/female body size ratio. Indeed, we did not detect any difference in egg fertilization success between small males paired with large and small females. Our results suggest that predictable cues of female reproductive value exist in common toads, thus meeting a prerequisite of the occurrence of male mate choice. Male mate choice, probably underestimated in anurans, may be particularly important in species where the breeding season is short and the number of mating events for a male is limited. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 92 , 755–762.