Divergence in male mating tactics between two populations of the soapberry bug: II. Genetic change and the evolution of a plastic reaction norm in a variable social environment

Many social behaviors are conditional, but behavioral comparisonsbetween populations do not normally distinguish genetic andenvironmental causation. As a result, the opportunity to testpredictions about the evolution of strategic conditionality(genotype x environment interaction) is lost. We apply theseconcepts in an examination of how interpopulation differencesin mean and variance of sex ratio have led to genetic differencesin the allocation of male effort to mate guarding versus nonguardingbetween genetically isolated populations of the soapberry bugin Oklahoma and Florida. We observed the mating behavior ofmales from the two populations at a series of experimental sexratios, and modeled their mating decisions as first-order Markovchains of independent mating states. Likelihood ratio testsof these behavioral sequences showed that the populations differedsignificantly in their response to sex ratio, and that onlymales from the variable environment (Oklahoma) altered theirbehavior in response to differences in female availability amongthe treatments. The flexible strategy of this population maybe adaptive and probably has evolved in response to sex ratiovariability.     

The adaptive significance of mate guarding in the soapberry bug,Jadera Haematoloma (Hemiptera: Rhopalidae)

Male soapberry bugs (Jadera haematoloma)face severe mating competition at the northern edge of their range due to male-biased adult sex ratios. Copulations lasting up to 11 days may serve a mate guarding function (encompassing four or more ovipositions), but copulation duration is highly variable, with some pairings lasting as little as 10 min. Data were gathered to describe factors that influence the reproductive costs and benefits of prolonged copulation. Estimated copulation durations (mean ± SD) were 20 ± 23 h in the lab and 50 ± 8 h in the field and were only weakly affected by sex ratio. Females mated for 5 min produced as many fertile eggs as those mated for 600 min laid; they became depleted of fertile sperm after about 25 days. In twicemated females, the first male's paternity was reduced by about 60%, and all females (N = 13) whose mates were removed experimentally mated again within an average of 6 min. The outcome of sperm competition on a perclutch basis was not highly predictable. The possibility of increased sperm displacement in longer copulations was not tested. Males often guarded females during oviposition and successfully defended them from intruding single males by recopulating. Such intrusions occurred in the majority of oviposition attempts observed in nature. Even though most females mated promiscuously, in a focal aggregation with a mean sex ratio of 2.2 ± 0.4 males/female, the interval between matings by males was commonly several days. Males appeared to respond facultatively to several aspects of the distribution and availability of females. The intensities of mating competition and sperm competition indicate that monogamous mate guarding should be favored over nonguarding in nature. Unpredicted brief. pairings may result from assessment by males of female reproductive value or of their own physical condition, or from female resistance.     

Rapidly evolving adaptations to host ecology and nutrition in the soapberry bug

With reciprocal rearing experiments, we tested the hypothesis that adaptive differences in host-use traits among soapberry bug populations have a genetic basis. These experiments were conducted with two host races from Florida, an ancestral-type one on a native host plant species and a derived one on a recently introduced plant species (colonized mainly post-1950), on whose seed crops this insect depends for growth and reproduction. Compared to the native host species, the introduced host produces larger seed crops over a much briefer annual period. Its seeds are also significantly higher in lipids and lower in nitrogen. The bug populations exhibit greater juvenile survivorship on their home hosts; that is, the derived population survives better on seeds of the introduced host than does its ancestral-type counterpart, and vice versa. Regardless of the rearing host, populations from the introduced host lay much smaller eggs, and fecundity measures show a more complex pattern than does survivorship: the ancestral-type population produces eggs at the same rate on each host, while the derived population is less fecund on the native host and exhibits enhanced fecundity on the introduced host. These results indicate that the population differences are evolved rather than host-induced. They appear to be adaptive responses to host differences in the spatial and temporal distribution of seed availability and nutritional quality, and show that increased performance on the alien host has evolved with surprising speed and magnitude, with concomitant reductions in performance on the original host.     

Female mating status does not affect male mating behavior in the West Indian sweetpotato weevil, Euscepes postfasciatus

Because multiple mating by females encourages sperm competition, the assessment of female mating status before insemination is important for males in order to avoid the risk of sperm competition or to intensify sperm competition. When interacting with females before sperm transfer, males can alter their mating tactics according to the risk or intensity of sperm competition. Information on how mating systems are associated with sperm competition is essential for sterile insect technique eradication programs, which depend on successful mating of released sterile males with wild females. We tested whether males of the West Indian sweetpotato weevil, Euscepes postfasciatus (Fairmaire) (Coleoptera: Curculionidae), adjusted their mating behavior in response to female mating experience and/or age. As virgin/young female weevils accepted males more easily than non-virgin/old females, assessing females before insemination can be adaptive for male weevils. We found that E. postfasciatus males were unable to adjust their mating tactics in response to female mating status. Although this mating strategy would be costly for individual male weevils, the ability in males to discriminate female mating status can prevent the chance of mating with already-mated females containing the sperm of wild male(s). Therefore, the mating tactics of male E. postfasciatus are advantageous for sterile insect technique eradication programs.     

Female egg dumping and the effect of sex ratio on male egg carrying in a coreid bug

Phyllomorpha laciniata Vill (Heteroptera, Coreidae) is uniqueamong terrestrial insects in that females glue eggs on the backsof other conspecifics. Egg carrying byP. laciniatamales haspreviously been considered as paternal care. We explored femaleoviposition with respect to previous mating experience of femalesand tested whether sex ratio affects male egg-carrying. Thehypothesis that male egg-carrying is a form of paternal carepredicts that a male should always accept eggs after matingwith a female. However, if male egg-carrying is a form of postcopulatorymate guarding rather than paternal care, egg carrying shouldincrease in the presence of other males. When two couples wereplaced together, females laid eggs on the backs of all individualsenclosed, including the backs of other females. However, whena female was accompanied by 2 males, 22 out of 26 females ovipositedon their mating partner. Thus, sexual competition rather thanpaternity alone, affects a male's eagerness to carry eggs. However,even if males sometimes carry their own eggs, females lay eggson the backs of all conspecifics they can easily acquire. Thus,egg carrying in P. laciniata is partially voluntary and partiallythe result of female egg dumping     

Correlates of reproductive success within alternative mating tactics of the common shrew

Male common shrews (Sorex araneus) adopt two discrete matingtactics. The most successful males, in terms of number of offspringfathered, are those that establish large overlapping home rangesin areas of high female density early in the breeding season.An alternative, less successful mating tactic is to travel longdistances in search of mating opportunities. This study is aninvestigation of correlates of reproductive success for malesadopting these different mating tactics. Reproductive successunder natural conditions was assessed using DNA fingerprinting,and survival of offspring was monitored in the field. The numberof offspring fathered by males with overlapping home rangeswas positively correlated with the number of female ranges overlappedduring the breeding season and with testes mass. The numberof offspring fathered by males that made long-distance movementswas positively correlated with their epididymal sperm counts.It is argued that competitively superior (overlapping) malesachieve high reproductive success by competing to maximize thenumber of females inseminated, whereas those adopting an alternativemating tactic instead compete largely via sperm competition,aiming to maximize insemination success with any particularfemale. There was no significant difference in the fluctuatingasymmetry (FA) of males adopting different mating tactics (FAwas measured as the difference in length of the paired lateralscent glands). Fluctuating asymmetry was not related to thenumber of offspring fathered by males adopting either matingtactic, but was significantly correlated with the proportionof male offspring fathered that survived to sexual maturity.Although apparently not correlated with mating success in thisspecies, FA may reflect some aspect of genetic quality thataffects offspring survival. [Behav Ecol 7: 334–340 (1996)]     

Evolution of alternative mating tactics: conditional versus mixed strategies

Intrasexual polymorphisms have evolved in a wide range of organisms.Most of them have been interpreted as the product of conditionalstrategies in which the tactic an individual adopts is determinedby some aspect of state (e.g., age, size, condition). However,there are a few examples that appear to represent an evolutionarilystable mixture of heritable pure strategies that are maintainedby frequency-dependent selection. In the present study, we producea model of a mating system with two morphs: a territorial morphand a sneak morph. By varying the costs and limits associatedwith conditional strategies, mating skew, and the proportionof matings obtained by sneaking males, we examine the conditionsthat favor the evolution of conditional versus pure strategies.Contrary to current thinking, our results show that as longas either costs or limits are greater than zero, conditionalstrategists are never able to entirely replace pure strategists,and equilibrium populations may frequently consist of a mixtureof conditional and pure strategists. Our results suggest thatconditional strategists will be most frequent at intermediatelevels of mating skew. Polymorphisms in which conditional strategistsare rare or absent are most likely to evolve when mating skewis extremely high, the costs and limits of plasticity are veryhigh, or the benefits of being conditional are very low. Thelimited data available suggest that high mating skew is probablythe most important factor.     

Trade-off between male and female allocation in the simultaneously hermaphroditic flatworm Macrostomum sp

Sex allocation theory for simultaneous hermaphrodites assumes a direct trade-off between the allocation of resources to the male and female reproductive functions. Empirical support for this basic assumption is scarce, possibly because studies rarely control for variation in individual reproductive resource budgets. Such variation, which can have environmental or genetic sources, can generate a positive relationship between male and female investment and can thus obscure the trade-off. In this study on the hermaphroditic flatworm Macrostomum sp. we tried to control for budget effects by restricting food availability in a standardized way and by using an inbred line. We then manipulated mating group size in a two-way design (two group sizes x two enclosure sizes) in order to induce phenotypic variation in male allocation, and expected to find an opposing correlated response in female allocation. The results suggest that we only managed to control the budget effects under some conditions. Under these the sex allocation trade-off emerged. Under the other conditions we found a strongly positive correlation between male and female allocation. We discuss possible causes for the observed differences.     

Independent effects of familiarity and mating preferences for ornamental traits on mating decisions in guppies

The avoidance of familiar individuals as mates can act to maximizethe benefits of polyandry or might help to minimize inbreedingin small or highly philopatric populations. As previous matesare also familiar, the effects of familiarity and mating historycan often be confounded. Here, we disentangle these effectson mating decisions in the guppy, Poecilia reticulata, and examinetheir influence on sexual selection. In 3 experiments, malesand females were 1) able to mate, 2) had visual and olfactorycontact, or 3) had visual contact only. Familiarity was successfullyacquired via visual cues, and females were in all cases morelikely to mate with unfamiliar than with familiar males, indicatingthat familiarity is a more important determinant of mating outcomethan mating history. Males did not court unfamiliar femalesany more than familiar females and did not differentially allocatesperm. Familiarity did not alter the strength of sexual selectionon male coloration: we found overall positive selection forbright, large males. Female preferences for unfamiliar malesand ornamental traits may therefore be largely independent.     

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.     

三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响

近年来越来越多研究表明,雄性产生精子(精液)也需付出代价。在多次交配的动物中,雄性为获得最大生殖潜力,必须依据配偶的质量策略性地调整每次交配的生殖投入。雄性策略性的生殖投入主要体现在两个方面,一是精子竞争(sperm competition),二是柯立芝效应(Coolidge effect)。目前精子竞争研究主要集中于昆虫类群,而柯立芝效应研究集中于高等脊椎动物,同时验证结果也时常与假说不一致。以多次交配的三突伊氏蛛为材料,以雄蛛交配行为为指标,在蜘蛛类群中探讨和验证雄性精子竞争强度假说和柯立芝效应。设定3个交配组合:2只雄蛛依次与1只雌蛛各交配1次(A组)、2只雄蛛依次与2只雌蛛各交配1次(B组)和1只雄蛛与1只雌蛛交配2次(C组),分析比较3个交配组合的三突伊氏蛛第1次交配和第2次交配在交配潜伏期、交配持续时间和交配回合数方面的差异,比较三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响,以此验证雄性精子竞争强度假说和柯立芝效应。研究结果表明A和B组的三突伊氏蛛第2次交配的交配潜伏期和交配持续时间显著长于第1次交配。同时,C组的三突伊氏蛛第1次交配的交配潜伏期和交配持续时间与第2次交配都没有显著差异。同时,A、B和C组的三突伊氏蛛第1次交配的交配回合数与第2次交配都没有显著差异。研究结果支持精子竞争强度假说,而不支持柯立芝效应。     

Decoy presentations as a means to manipulate the risk of extrapair copulation: an experimental study in a semicolonial raptor, the Montagu's harrier (Circus pygargus)

Mate guarding and frequent copulations are two alternative paternity assurance strategies found in birds. In species with intensecourtship feeding, like raptors, the "frequent copulation"strategy is expected because male food provisioning conflictswith mate guarding. We evaluated experimentally the paternityassurance behavior of a semicolonial raptor, the Montagu'sharrier Circus pygargus, using decoy presentations to simulateterritorial intrusions. Breeding pairs were exposed to maleand female decoys at different periods during the female's reproductive cycle. Agonistic responses to decoys were intra-sexual,and the timing and intensity of male attacks toward male decoyssupported responses related to the risk of extrapair copulation(EPC): Male aggression peaked during the presumed fertile periodand almost disappeared after clutch completion. During thefertile period, copulation rate was significantly higher, andcopulations lasted longer, during male decoy presentations than during controls. Males also spent more time close to the femaleduring male decoy presentations compared to controls, bothduring the early prelaying and fertile periods, but not duringincubation. In the fertile period, males also increased presencetime close to the female in the hour following the removal of the male decoy. Conversely, female decoy presentations hadno significant effect on copulatory behavior or male presencetime. These results showed that the risk of EPC can be experimentallymanipulated by the means of decoy presentations, simulatingmale territorial intrusions, and that male Montagu's harriersincrease their short-term copulation frequency and female surveillancewhen they perceive themselves at an increased EPC risk.     

Determinants of male ejaculate investment in the cotton bollworm Helicoverpa armigera: mating history,female body size and male age

Many studies demonstrate that ejaculate size may be influenced by male condition, female quality and the risk or intensity of sperm competition. In the present study, the effect of male and female conditions, male mating history and female mating status on ejaculate sperm numbers in the polyandrous moth Helicoverpa armigera is examined. A large variation in ejaculate size is found and, although female body size and male age influence ejaculate size, female age and copula duration do not. Both male and female mating histories have significant effects on ejaculate sperm numbers. Males reduce ejaculate expenditure in successive matings but deliver significantly more apyrene and eupyrene sperm to nonvirgin than to virgin females.     

Conflict over multiple-partner mating between males and females of the polygynandrous common lizards

The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple-partner mating. This suggests that the population sex ratio may affect multiple-partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male-biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male-biased populations females suffered from reduced reproductive success compared to female-biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male-biased populations showed disproportionately more mating scars, indicating that polyandrous females of male-biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.     

Use of female nest characteristics in the sexual behaviour of male sockeye salmon

On three island beaches in Iliamna Lake, Alaska, large numbers of male sockeye salmon gathered and spawned in artificial excavations that mimicked a female's nest immediately prior to spawning, while apparently ignoring the control site. The number of males attracted was correlated positively with changes in the operational sex ratio. In contrast, on the mainland beach examined, no reaction to the artificial nests was apparent. The results are discussed in terms of mate searching behaviour by males, the duration of the spawning period, and associated selection pressures on males to use characteristics of their environment that provide information on availability of females.     

Inhibition of female mating by male accessory gland substances in the ground beetle Leptocarabus procerulus

The ground beetle Leptocarabus procerulus (Chaudoir) possesses seminal substances that have a physical function to form mating plugs and a physiological function to induce female refractory behaviour, which act together to hinder female remating. Little is known about the physiological properties of the substances inducing female refractory behaviour, especially with respect to their secretory organ, dose‐dependency, molecular characteristics and the effect of female maturity. By injecting male‐derived substances into females, substances that induce female refractory behaviour are shown to be produced in the male accessory gland but not in the testis. Injection of extracts from the accessory gland increases the female refractory period at moderate doses but not at lower or higher doses. By contrast, injection of extracts from the testis reduces the female refractory period at high doses. The lack of an effect of accessory gland substances at higher doses could be the result of an anomalous effect of unnaturally large doses of seminal products by direct injection, the toxicity of seminal substances that deter female responses, or counteraction by injected substances that promote female receptivity. The accessory gland substances lose their activity when heated, although the testis substances do not. Females without mature eggs tend to reject mating entirely, although variation in the number of mature eggs (one or more) is not associated with the female refractory period, indicating the limited effect of female reproductive maturity. These findings may help to clarify the physiological basis of the evolution of the elaborated male mating behaviour in L. procerulus.     

State-dependent male mating tactics in the grey seal: the importance of body size

The purpose of this study was to examine the importance of bodysize and body composition as determinants of conditional matingtactics exhibited in male grey seals. We combined behavioralobservations with measures of energy expenditure and successon 42 known-age individuals during the breeding seasons of 1997–2001at Sable Island, Canada. Males with a large body mass arrivedat the breeding grounds with more body fat and body energy andcatabolized less body protein than smaller males. Males consumed1.9 ± 0.2 MJ day^–1, and those with a smaller percentageof body fat had higher rates of food energy intake. The amountof body energy on arrival was positively correlated with theduration of the breeding period. Males that exhibited the primarymating tactic of consortship were heavier, had absolutely morebody fat and body energy, and sustained breeding longer thanthose males that did not exhibit the primary tactic. Amongstall males, body mass showed a quadratic relationship with thenumber of female consorts mated and the estimated number ofpups sired. Thus, intermediate-sized males mated with the mostconsorts and achieved the highest success. Intermediate bodysize may be optimal during breeding due to greater agility inmale combat. Body size was an important determinant of matingtactics used by male grey seals. A large body size providedan energetic advantage of greater endurance while an intermediatebody size may provide greater competitive ability in acquiringconsortships.