Sexual cannibalism and sperm competition in the golden orb-web spider Nephila plumipes (Araneoidea): female and male perspectives

Mating systems are frequently shaped by conflicts over reproductive interests between males and females. Sexual cannibalism canbe an especially dramatic manifestation of such conflicts.However, the resolutions of this conflict differ among sexuallycannibalistic spider species. Cannibalism may be in the interestof both sexes when females consume males as a foraging decisionto improve fecundity and/or males sacrifice their bodies toincrease fertilization success. In other species, females exertsequential choice of partner by selectively terminating copulationthrough cannibalism while males fail to obtain a paternityadvantage. Here, we investigate the adaptive value of cannibalismin the orb-web spider Nephila plumipes where 60% of males donot survive copulation. Virgin females in poor condition aremore frequently cannibalistic and more likely to kill largemales, but the frequency of cannibalism among mated femalesis not influenced by these factors. Instead, males that matewith mated females increase their fertilization success bybeing cannibalized. Cannibalized males generally mate for longer,but longer copulations correspond with increased paternity onlyin mated females. The amount of sperm from particular malesthat a female stored was not influenced by any of the measuredvariables. The number of sperm stored was not related to paternity,nor was there any detectable reduction in sperm number afterfemales had reproduced. Our data suggest that the conflict between the sexes differs between virgin and mated females.Females should always cannibalize a male, but males only gainfrom cannibalism when mating with mated females, not when matingwith virgin females. Interestingly, the frequencies of cannibalismare not different in matings with virgin or mated females.     

Foraging strategies of Eriophora transmarina and Nephila plumipes (Araneae: Araneoidea): Nocturnal and diurnal orb-weaving spiders

Abstract The foraging behaviour, web characteristics and prey availability of two sympatric orb-weaving spiders, Nephila plumipes and Eriophora transmarina (Araneae: Araneoidea), are compared. The spiders are similarly sized but have different temporal foraging patterns. Nephila plumipes spins a relatively permanent web and captures most of its prey during the day. Eriophora transmarina only forages at night, spinning a new web every night and usually dismantling it at dawn. These different foraging activities are most likely to be responsible for the observed differences in the types and rates of prey capture: E. transmarina captured mostly Lepidoptera that were more abundant at night than during the day, while N. plumipes captured mostly Hymenoptera that were more abundant during the day than at night. While nocturnal E. transmarina have less time available for foraging than the diurnal N. plumipes, the former has a substantially higher nocturnal prey capture rate. We argue that the difference between the species in their prey capture rates are likely to be due to differences in the architecture of their webs.     

Sexual cannibalism, competition, and size dimorphism in the orb-weaving spider Nephila plumipes Latreille (Araneae: Araneoidea)

The degree and direction of sexual dimorphism varies widely,but in several taxa of orb-weaving spiders, including Nephila,males may be less than one-tenth the size of females. This differenceis commonly attributed to selection through precopulation sexualcannibalism: females may either fail to detect very small males,or ignore them as potential prey items. However, there is oftenthe potential for male-male competition in these species becauseseveral males can be found on the web of a single female. Weinvestigated experimentally the effects of sexual cannibalismand male-male competition on male body size and hence sexualdimorphism in the Australian golden orb-weaver (Nephila plumipes).Small males were less likely to be detected and cannibalizedthan larger males. However, larger males excluded small malesfrom the central hub of the web, where mating takes place. Theconflicting effects of sexual cannibalism and male-male competitionmay be responsible for the relatively large variation in malebody size in this species.     

Risky mate search and male self-sacrifice in redback spiders

Male redback spiders twist their abdomens onto the fangs oftheir mates during copulation and, if cannibalized (65% of matings),increase their paternity relative to males that are not cannibalized.The adaptive male sacrifice hypothesis proposes that this increasedreproductive payoff from a single mating outweighs the residualreproductive value of a cannibalized male, because high mortalityduring mate searching restricts alternative mating opportunities.It has been reported that redback male residual reproductivevalue is low because males are functionally sterile after onemating—a putative intrinsic constraint that could arguablyfavor self-sacrifice in the absence of ecological restrictionson multiple mating. However, sterility and self-sacrifice mayboth arise as aspects of a terminal investment strategy if theprobability of multiple mating is sufficiently low. Here I reportfield data that support the adaptive male sacrifice hypothesis.More than 80% of redback males die without finding a potentialmate in nature. Data from two observational field studies andone release experiment suggest that in the absence of cannibalism,male redbacks would expect fewer than one mating opportunityin a lifetime. This expectation was not significantly higherfor a large male or one in good condition. A simple quantitativeanalysis confirms that even if males are assumed to be fertilethroughout life, the measured mortality rate during mate searchin combination with previously documented paternity benefitsof cannibalism is sufficient to ensure that self-sacrifice isadaptive for male redback spiders.     

Copulation patterns in the golden orb-web spider Nephila madagascariensis

A consequence of multiple mating by females can be that the sperm of two or more males directly compete for the fertilisation of ova inside the female reproductive tract. Selection through sperm-competition favours males that protect their sperm against that of rivals and strategically allocate their sperm, e.g., according to the mating status of the female and the morphology of the spermatheca. In the majority of spiders, we encounter the otherwise unusual situation that females possess two independent insemination ducts, both ending in their own sperm storage organ, the spermatheca. Males have paired mating organs, but generally can only fill one spermatheca at a time. We investigated whether males of the African golden orb-web spider Nephila madagascariensis can prevent rival males from mating into the same spermatheca and whether the mating status of the female and/or the spermatheca causes differences in male mating behaviour. There was no significant difference in the duration of copulations into unused spermathecae of virgin and mated females. We found that copulations into previously inseminated spermathecae were generally possible, but shorter than copulations into the unused side of mated females or with virgins. Thus, male N. madagascariensis may have an advantage when they mate with virgins, but cannot prevent future males from mating. However, in rare instances, parts of the male genitals can completely obstruct a female genital opening.     

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.     

Reliable acoustic cues for female mate preference in a katydid (Scudderia curvicauda, Orthoptera: Tettigoniidae)

The call of male Scudderia curvicauda (Orthoptera: Tettigoniidae)consists of a series of phrases, and each phrase contains syllables.Females respond to the male signal with ticks that follow malephrases after a specific period of time. Pair formation takesplace after males locate the female using her response sounds.Repeated recordings of males revealed that the average numberof syllables produced per phrase was a table, within-male parameterand that this parameter was a reliable predictor of male size(pronotum length). Thus, phrase length could be a reliable cueby which females evaluate males. We presented virgin femaleswith a sequential choice of two tape-recorded male calls thatdiffered only in the mean number of syllables produced per phrase.Two different playback tapes were used, and each female wastested on each of 5 consecutive days with the same playbacktape. Females responded more often and with a greater numberof ticks to calls containing more syllables per phrase, andthis preference was maintained throughout the testing period.Male size was a poor predictor of the size of the spermatophorefood-gift produced by the male; therefore, females are probablynot selecting males for this attribute. For one of the playbacktapes, there was a significant increase in female responsivenessover several playback trials, suggesting that females may employa falling-threshold tactic with respect to mate preference.     

Male-male competition and mating success in the orb-web spider,Nephila clavata,with reference to temporal factors

Seasonal occurrence patterns of adults of both sexes, intensity of male-male interactions, and mating success in the spider,Nephila clavata, were examined in the field. Adult males began to attend female webs about 2 weeks before female maturation. Large adult males were abundant in the early breeding season, but small males increased later in the season. From the distribution of males among female webs and size relationship of males within a web, male-male interactions seemed to be more intense when most females were still subadult. This was verified by a field experiment in which males were artificially introduced to female webs that were attended by other males. It was found that the probability of introduced males remaining on subadult female webs was lower than that on adult webs. As mating occurred mostly in the period shortly after the female final molt and first male sperm precedence was known in all spiders reported so far, intense male-male competition on subadult female webs seemed to be reasonable. Male longevity had an important influence on the mating success of males with just-molted females. Mating success was also affected by the relative body size of males present in a given period. Since larger males occupied the position closest to females within a web and stayed there longer, relative body size appeared to influence mating success through male-male competition. Female body size at maturation declined with time; hence, males that attained sexual maturity earlier had the advantage of mating with larger and more fecund females. Therefore, early maturation as well as larger size seem to be two important trairs influencing the reproductive success of males.     

Male mate preference and size-assortative pairing in the convict cichlid

Male convict cichlids Cichlasoma nigrofasciatum presented three females simultaneously were found to prefer larger females, even if a female's size exceeded their own. This indicates that some mechanism other than male choice, such as female choice or intrasexual competition, must contribute to male-larger assortative pairing in convict cichlids. Despite a preference for larger females, males continued to consort with smaller females when available, and a females attractiveness was a function of her size relative to other females.     

Fine structure of the chelicera in the spider Nephila clavata

The fine structural characteristics of the biting apparatus in the orb‐web spider Nephila clavata were studied using scanning electron microscopy. The main biting apparatuses of spiders are the chelicerae and cheliceral fangs in the cephalothorax. The chelicera of N. clavata is that of the jack‐knife (folding knife) type, which is composed of two segments, and has a labidognathous form that moves at right angles to the body axis. Each chelicera bears a hinged fang that folds into a cheliceral groove. The tips of the fangs are quite sharp, and the spider's body is well adapted to driving the fangs into prey. Just below the fang, each side of the cheliceral groove is covered with a total of seven cuticular teeth (four promarginal teeth and three retromarginal teeth) in two rows. The cheliceral fang has a single aperture at the tip of the posterior surface, and the lower margin of the fang which meets the promarginal teeth is a saw‐like groove. Fine structural observation reveals that each fang has a single venom pore, and each cuticular depressive area on the cheliceral groove has two different types of surface pit. Approximately 40 to 50 spiky protrusions were counted at the cheliceral groove, to hold prey tightly.     

Fine structure of the CNS ganglia in the geometric spider Nephila clavata (Araneae: Nephilidae)

As web spiders usually hang with their head downward, geometrical differences in body position could affect the organization of their central nervous system (CNS). Nevertheless, most of our knowledge of spider's CNS is dependent on what has been revealed from wandering spiders. To fill the gap, we describe here the fine structural organization of the ganglionic neurons and nerves in the geometric orb web spider Nephila clavata. Nerve cells in the supraesophageal ganglion in N. clavata are packed in the frontal, dorsal and lateral regions, but the nerve cells of the subesophageal mass are only restricted to the ventral and ventrolateral regions. High resolution transmission electron microscopy (TEM) reveals the fine structural details of the neuroglial cells and the neuronal cells which have a conspicuous Golgi apparatus, rough ER, free ribosomes and well‐developed mitochondria. Comparing fine structural characteristics of the CNS ganglia with those of wandering spiders in most respects, it has been revealed that the geometrical difference may affects to the arrangement of receptors in the central body known as an important association center for web building behavior. In particular, remarkable differences can be detected in the protocerebral area by the extraordinary development of the central body including absence of the globuli and associated mushroom bodies.     

Long-term persistence of exaggerated ornaments under Fisherian runaway despite costly mate search

Exaggerated ornaments often evolve due to the mating preferences of the opposite sex. Genetic correlations between preferences and ornaments can lead both traits to elaborate dramatically in tandem, in a process known as ‘Fisherian runaway’. However, in most previous models of Fisherian runaway, elaborate ornaments are not expected to persist when preferences are consistently costly to the choosing sex. In contrast, we show here that exaggerated male ornaments can be maintained long term even when females must pay a cost to choose their mates. Preferences per se are not costly in our model, but females can only act on their preferences by investing resources in mate search. We predict that mate search effort should decrease with the cost of sampling additional mates and increase with the number of possible ornaments that females can choose from. The potential for multiple exaggerated ornaments to coexist depends on subtleties of their cost structure: strict trade-offs (additive costs) favour sequential ornament evolution, whereas looser trade-offs (multiplicative costs) allow for coexistence. Lastly, we show that pleiotropy affecting both ornaments and preferences makes it difficult for Fisherian runaway to initiate, increasing the evolutionary time until ornamentation. Our model highlights the important but neglected role of mate search effort in sexual selection.     

Previous experiences shape adaptive mate preferences

Existing models of mate choice assume that individuals haveperfect knowledge of their own ability to attract a mate andcan adjust their preferences accordingly. However, real animalswill typically be uncertain of their own attractiveness. A potentiallyuseful source of information on this is the feedback from previousencounters with potential mates. Here, we develop a dynamicmodel of mutual mate choice in which both males and femalesare initially ignorant of their own attractiveness. Individualssequentially sample potential mates and retain some informationabout the outcome of these encounters (e.g., the number of timesthey are accepted or rejected). We use a simplified processof mutation and selection to evolve an adaptive strategy formate choice under these conditions. The stable strategy we findis the one in which individuals are sensitive to this previousexperience, adjusting their mate preferences according to theinterest received from members of the opposite sex. In general,experiences of rejection tend to reduce choosiness, whereasexperiences of acceptance tend to increase it. Sensitivity toprevious experiences allows individuals to exercise a prudentmate-choice strategy in which their preferences are graduallytuned to their prospects on the mating market. This flexibilityis based on simple rules and does not require sophisticatedcognitive abilities. Our basic predictions can be tested insystems where both males and females are choosy, and it is possibleto manipulate the level of interest shown by potential mates.     

Feeding rate may affect dispersal in the orb-web spider Nephila clavata

Population parameters of the orb-web spider Nephila clavata were estimated at two sites with different spider densities (for 2 successive years at the high density site and 1 year at the low density site), and the relationship between survival rate and feeding conditions was examined. The rate of decrease of population density was almost constant over time and nearly the same at the two sites. Daily survival rate (sum of the effects of mortality and emigration) was low during August to early September and increased markedly thereafter. Daily immigration rate (number of immigrants/number of residents) was high during August to early September. Since there were strong negative correlations between survival and immigration rates, low survival rate seems to be caused by a high rate of emigration. Strong positive correlations were found between survival rate and feeding frequency (mean percent observed feeding). Analysis of covariance revealed that the parameters of the regression between survival rate and feeding frequency did not differ significantly among three occasions. These results suggest that feeding condition has a significant influence on dispersal activity of populations in this spider.     

Female mate preference explains countergradient variation in the sexual coloration of guppies (Poecilia reticulata)

We tested the hypothesis that mate choice is responsible for countergradient variation in the sexual coloration of Trinidadian guppies (Poecilia reticulata). The nature of the countergradient pattern is that geographical variation in the carotenoid content of the orange spots of males is counterbalanced by genetic variation in drosopterin production, resulting in a relatively uniform pigment ratio. A female hue preference could produce this pattern, because hue is the axis of colour variation most directly affected by the pigment ratio. To test this hypothesis, we crossed two populations differing in drosopterin production and produced an F(2) generation with variable drosopterin levels. When the carotenoid content of the orange spots was held constant, female guppies preferred males with intermediate drosopterin levels. This shows that females do not simply prefer males with greater orange spot pigment content; instead, the ratio of the pigments also affects male attractiveness. To our knowledge, this is the first direct evidence for a hypothesized agent of countergradient sexual selection.     

Ultraviolet vision and mate choice in the guppy (Poecilia reticulata)

Ultraviolet (UV) vision is well documented for many speciesof vertebrates. UV cues are known to be used in foraging, navigationand in mate choice. We conducted a series of behavioral experimentsto investigate the role of UV perception in mate choice inboth female and male guppies (Poecilia reticulata). In ourexperiments the visual appearance of potential mates was manipulatedusing either UV transmitting (UV+) or UV blocking (UV-) filters.Female guppies significantly preferred UV+ males. Male guppiestended to prefer UV- females, but their preferences were marginallynonsignificant. Further experiments investigating the roleof luminance, indicate that UV wavelengths are probably beingused for color discrimination rather than for detecting differencesin brightness. These experiments raise the possibility thatUV is used in mate assessment in different ways by male andfemale guppies. This may reflect the different strategies thatthe two sexes have in order to maximize reproductive success.To our knowledge, these are the first data showing that UVis used by any fish species in mate selection.     

Female mate choice in vervet monkeys (Cercopithecus aethiops sabaeus)

Female mate choice was examined in a captive group of vervet monkeys (Cercopithecus aethiops sabaeus). Male-female interactions were examined under both dyadic and group conditions to determine whether females mate with different males under the two conditions. Results showed that all females preferred to mate with the alpha male under both dyadic and group conditions. Alpha females, however, were more successful than subordinate females in rejecting the sexual solicitations of subordinate males. Thus female dominance status played an important role in determining the degree to which females exercised mate choice.