Even Weak Males Help Their Neighbours: Defence Coalitions in a Fiddler Crab

Large male fiddler crabs sometimes help smaller neighbours to defend their territories against intruders. These coalitions occur when the helper is likely to defeat the intruder (helper larger than intruder) and the neighbour is likely to lose his territory without help (intruder larger than neighbour). Previous studies of coalitions have excluded males with regenerated claws. Such claws are weaker weapons that make the bearer competitively inferior. Here, we show that male Uca annulipes with regenerated claws are as likely as males with original claws to help their neighbours in territory defence, even though, as weaker males they potentially pay greater costs, being more likely to lose their undefended burrow. We suggest that males with regenerated claws gain greater benefits from retaining a current, small neighbour and that, as in non‐coalition fights, the regenerated claw acts as a visual bluff in the early stages of combat. Furthermore, we show that intruders with regenerated or original claws are equally likely to be attacked by a ‘helping’ neighbour. This bolsters the argument that males cannot visually differentiate between original and regenerated claws.     

What are the consequences of being left-clawed in a predominantly right-clawed fiddler crab?

Male fiddler crabs (genus Uca) have an enlarged major claw that is used during fights. In most species, 50% of males have a major claw on the left and 50% on the right. In Uca vocans vomeris, however, less than 1.4% of males are left-clawed. Fights between opponents with claws on the same or opposite side result in different physical alignment of claws, which affects fighting tactics. Left-clawed males mainly fight opposite-clawed opponents, so we predicted that they would be better fighters due to their relatively greater experience in fighting opposite-clawed opponents. We found, however, that (i) a left-clawed male retains a burrow for a significantly shorter period than a size-matched right-clawed male, (ii) when experimentally displaced from their burrow, there is no difference in the tactics used by left- and right-clawed males to obtain a new burrow; however, right-clawed males are significantly more likely to initiate fights with resident males, and (iii) right-clawed residents engage in significantly more fights than left-clawed residents. It appears that left-clawed males are actually less likely to fight, and when they do fight they are less likely to win, than right-clawed males. The low-level persistence of left-clawed males is therefore unlikely to involve a frequency-dependent advantage associated with fighting experience.     

Male mating success in a fiddler crab: a lesson in sample sizes

Autotomy and regrowth of a body part occurs in many animal species. It is costly to regrow the limb and there are often additional long-term costs in, for example, limb strength, foraging efficiency and even mating success. In the fiddler crab Uca mjoebergi, 7 % of males have autotomized and regrown their large claw at some point in their lives. Previous work has shown that there is a great disadvantage to having a regenerated claw. While these males are able to attract mate-searching females to visit them, none of the 84 males observed to have mated in previously collected data had regenerated claws. Since females’ final mate choice is based on burrow structure, it was assumed that males with regenerated claws had poorer burrows. Here we show that, by finding only three cases of a female mating with a regenerated claw male, that there is, in fact, no mating disadvantage to having a regenerated claw. We also show that the burrows of males with regenerated claws are no different than those of orginal-clawed males. This is a very clear reminder that sample size matters, especially when dealing with rare events.     

It takes two: Seasonal variation in sexually dimorphic weaponry results from divergent changes in males and females

Sexually dimorphic weaponry often results from intrasexual selection, and weapon size can vary seasonally when costs of bearing the weapon exceed the benefits outside of the reproductive season. Weapons can also be favored in competition over nonreproductive resources such as food or shelter, and if such nonreproductive competition occurs year‐round, weapons may be less likely to vary seasonally. In snapping shrimp (Alpheus angulosus), both sexes have an enlarged snapping claw (a potentially deadly weapon), and males of many species have larger claws than females, although females are more aggressive. This contrasting sexual dimorphism (larger weaponry in males, higher aggression in females) raises the question of whether weaponry and aggression are favored by the same mechanisms in males and females. We used field data to determine whether either sex shows seasonal variation in claw size such as described above. We found sexual dimorphism increased during the reproductive season due to opposing changes in both male and female claw size. Males had larger claws during the reproductive season than during the nonreproductive season, a pattern consistent with sexual selection. Females, however, had larger claws during the nonreproductive season than during the reproductive season—a previously unknown pattern of variation in weapon size. The observed changes in female weapon size suggest a trade‐off between claw growth and reproduction in the reproductive season, with investment in claw growth primarily in the nonreproductive season. Sexually dimorphic weaponry in snapping shrimp, then, varies seasonally due to sex differences in seasonal patterns of investment in claw growth, suggesting claws may be advantageous for both sexes but in different contexts. Thus, understanding sexual dimorphisms through the lens of one sex yields an incomplete understanding of the factors favoring their evolution.     

THE DESIGN OF A BEAUTIFUL WEAPON: COMPENSATION FOR OPPOSING SEXUAL SELECTION ON A TRAIT WITH TWO FUNCTIONS

Male fiddler crabs, genus Uca, have one greatly enlarged claw with which they court females and threaten and fight other males. Longer claws are more effective signals but are thought to be less effective weapons because the relative closing force at the tip of the claw decreases with claw length. We studied claw morphology and fighting in Uca terpsichores and Uca beebei and found a mechanism that may resolve opposing selection for signaling and fighting ability. When males fought they delivered gripping forces not at the tips but at the tubercles on the inner margins of their claws’ fingers. As claws grow, these tubercles remain relatively close to the apex of the gape. Consequently, the mechanical advantage that governs the forces that can be delivered at these tubercles decreases only slightly with increasing claw length allowing the claw to be an effective signal and a powerful weapon. Animal weapons are exceptionally diverse in form and detail of armature and the causes of this diversity are poorly understood. We suggest that the designs of weapons may often reflect compensatory patterns of growth and placement of armature that enhances the weapon's overall utility for multiple uses in competition for mates.     

Post-autotomy claw regrowth and functional recovery in the snapping shrimp Alpheus angulosus

The ability to regenerate lost tissues, organs or whole body parts is widespread across animal taxa; in some animals, regeneration includes transforming a remaining structure to replace the one that was lost. The transformation of one limb into another involves considerable plasticity in morphology, physiology and behavior, and snapping shrimp offer excellent opportunities for studying this process. We examined the changes required for the transformation of the small pincer to a mature snapping claw in Alpheus angulosus. First molt claws differ from mature claws in overall shape as well as in morphology related to snapping function; nonetheless, shrimp with first molt claws do produce snaps. While most shape variables of second molt claws do not differ significantly from mature claws, the plunger (structure required for snap production) does not reach mature size until the third molt for females, or later for males. Thus, the pincer claw can be transformed into a functional snapping claw in one molt, although both the underlying morphology and superficial shape are not fully regenerated at this stage. The rapid production of a functional snapping claw that we observe in this study suggests that this particular function is of significant importance to snapping shrimp behavior and survival.     

Moving in fast waters: the exaggerated claw gape of the New River crayfish (Cambarus chasmodactlyus) aids in locomotor performance

Humans are inherently fascinated by exaggerated morphological structures such as elk antlers and peacock trains. Because these traits are costly to develop and wield, the environment in which they are used can select for specific sizes or shapes to minimize such costs. In aquatic environments, selection to reduce drag can constrain the form of exaggerated structures; this is presumably why exaggerated morphologies are less common in aquatic environments compared to terrestrial ones. Interestingly, some crayfish species possess claws with an exaggerated gape between their pinching fingers, but the function of this claw gape is unknown. Here, I describe and test the function of the exaggerated claw gape of the New River crayfish, Cambarus chasmodactylus. Specifically, I test the hypothesis that the claw gape aids in movement against flowing currents. I found that both claw size and gape size were sexually dimorphic in this species and that males have disproportionately larger gapes compared to females. By experimentally covering their claw gape and testing crayfish locomotor performance, I found that individuals with their gape blocked were 30% slower than crayfish with a natural gape. My results highlight a unique adaptation that compensates for wielding an exaggerated structure in aquatic environments.     

The effect of claw size and wave rate on female choice in a fiddler crab

How do females select a mate when they have mating preferences for multiple male traits? In experimental studies, female fiddler crabs (Uca mjoebergi) show a strong preference for males with larger claws and higher wave rates. In the field, there is no correlation between male claw size and observed wave rate. Here we document natural mating behaviour and show that females approach males who wave at a higher rate than nearby competitors. On average, an approached male had a significantly larger claw than his two nearest neighbours but did not differ in size from his two closest waving competitors. In general, smaller males were less likely to wave at approaching females. Females therefore approached mates based directly on wave rate but, because smaller males were less likely to wave, this indirectly resulted in female choice for larger than average males. Our study raises two issues. First, how do we relate the field results to previous experimental studies showing a female preference for larger claws? Second, in U. mjoebergi, males defend smaller neighbours against intruders. Our study suggests that one benefit of such defence coalitions is to decrease the number of immediate competitors present during female mate choice by retaining smaller neighbours.     

Sex, size and colour in a semi-terrestrial crab, Heloecius cordiformis (H. Milne Edwards, 1837)

We investigated the relationship between sex, size and colour in the little studied Australian endemic semaphore crab, Heloecius cordiformis, and related it to the crabs' social system with the aim of identifying the potential signalling function of claw colour.Equal sampling of crabs from all size classes revealed a strong relationship between sex, size and claw colour. Purple-clawed males were larger and had larger claws than pink-, orange- or green-clawed males. Male claws showed positive allometric growth: relative to body size, purple-clawed males had larger claws. The largest females had pink claws; the few with purple claws were no larger than immature green-clawed crabs. Female claws grow isometrically with the body so the relative claw size did not differ among the female colour classes. Quantitative measurements of claw colour revealed spectral differences between these subjectively described colours. The purple claws typical of large males also contrasted more strongly against the mudflat background than the other colours.Heloecius copulate outside female-owned burrows and probably within male-owned burrows. The male's waving display, in which both claws are raised and lowered, may feature in both mating strategies: as a territorial display and to attract wandering females. Large males are competitively superior so size, and potentially colour, are important in territorial disputes and may also feature in mate choice.     

An experimental test of whether cheating is context dependent

Microbial cells rely on cooperative behaviours that can breakdown as a result of exploitation by cheats. Recent work on cheating in microbes, however, has produced examples of populations benefiting from the presence of cheats and/or cooperative behaviours being maintained despite the presence of cheats. These observations have been presented as evidence for selection favouring cheating at the population level. This apparent contradiction arises when cheating is defined simply by the reduced expression of a cooperative trait and not in terms of the social costs and benefits of the trait under investigation. Here, we use two social traits, quorum sensing and iron‐scavenging siderophore production in Pseudomonas aeruginosa, to illustrate the importance of defining cheating by the social costs and benefits. We show that whether a strain is a cheat depends on the costs and benefits associated with the social and abiotic environment and not the absolute expression of a cooperative trait.     

Quorum-sensing and cheating in bacterial biofilms

The idea from human societies that self-interest can lead to a breakdown of cooperation at the group level is sometimes termed the public goods dilemma. We tested this idea in the opportunistic bacterial pathogen, Pseudomonas aeruginosa, by examining the influence of putative cheats that do not cooperate via cell-to-cell signalling (quorum-sensing, QS). We found that: (i) QS cheating occurs in biofilm populations owing to exploitation of QS-regulated public goods; (ii) the thickness and density of biofilms was reduced by the presence of non-cooperative cheats; (iii) population growth was reduced by the presence of cheats, and this reduction was greater in biofilms than in planktonic populations; (iv) the susceptibility of biofilms to antibiotics was increased by the presence of cheats; and (v) coercing cooperator cells to increase their level of cooperation decreases the extent to which the presence of cheats reduces population productivity. Our results provide clear support that conflict over public goods reduces population fitness in bacterial biofilms, and that this effect is greater than in planktonic populations. Finally, we discuss the clinical implications that arise from altering the susceptibility to antibiotics.     

Composition of external setae during regeneration and transformation of the bilaterally asymmetric claws of the snapping shrimp,Alpheus heterochelis

The paired thoracic chelipeds or claws of adult snapping shrimp, Alpheus heterochelis, are bilaterally asymmetric, consisting of an enlarged and elaborate, sound-producing major (snapper) claw and a much smaller minor (pincer) claw. These paired claws vary in the composition of their external sensilla. Both possess long serrulate and simple short setae but the snapper also have plumose setae and long serrulate setae on the plunger. The pincers differ in having short serrulate setae and, in males alone, a prominent fringe of plumoserrate setae. During regeneration of each claw type, these setal structures are gradually added over three molts to reach the pristine condition. The long serrulate and simple short setae appear first, being seen in intermolt limb buds and commonly in both claws. Setae exclusive to each claw, i.e., plumoserrate and short serrulate in the pincer and plumose and long serrulate on the plunger in the snapper, appear sparsely in either the regenerated 1st or 2nd postmolt claw, they proliferate in the subsequent 2nd or 3rd postmolt claw. Transformation of the pincer claw to the snapper type begins in the 1st postmolt stage with the loss of pincer setae and addition of snapper setae and is completed by the 3rd postmolt stage. Since changes in composition of the external sensilla are restricted to postmolt stages, the underlying hypodermis is presumably being remodeled during proecdysis.     

Variation in safety factors of claws within and among six species of Cancer crabs (Decapoda: Brachyura)

To better understand how safety factors of biological structures evolve, we examined the frequency of claw failure, and the intra‐ and interspecific patterns of variation in maximum biting force and breaking strength in the claws of six species of Cancer (Linnaeus) crabs that live in sympatrv along the coast of the northeastern Pacific: C. antennarius, C. branneri, C. gracilis, C. maguter, C. oregonensis and C. productus. Although the breakage frequencies in natural populations were similar among species (6%), they were higher than predicted based on failure probabilities calculated from laboratory measurements of biting force and breaking strength for healthy pristine claws. The incidence of claw damage was correlated with the degree of wear, suggesting that claws later in the intermolt interval were more likely to fail. Within species, safety factors increased from 3.1 to 4.6 with increasing instar number due primarily to a decline in muscle stress (force per unit area of apodeme). Surprisingly, the lower maximum muscle stress generated by later instars appeared to be due to behavioral restraint, since it was not accompanied by relatively lower muscle mass. In addition, among individuals of the same claw size, lower breaking forces were correlated with lower maximum biting force, and both were correlated with lighter cuticle and closer muscle mass, suggesting a coupling that maintains a more stable safety factor over the moult cycle. In some species, size‐adjusted maximum biting forces were higher for males than females, but this paralleled differences in breaking strength, so safety factors did not differ between the sexes. Among the six Cancer species, one exhibited an unusually high safety factor (C. oregonensis, 7.4) and another an unusually low one (C. maguter, 2.6). The remaining four species were similar to each other and exhibited an intermediate safety factor (3.6). From a phylogenetic perspective, the species with more extreme safety factors appeared to be derived from a common ancestor with an intermediate safety factor. From an ecological perspective, species more closely associated with rocky substrata, and presumably a higher incidence of hard‐shelled prey, exhibited higher safety factors. But safety factors were also correlated with relative claw size, and sexual dimorphism in claw size. Although we cannot say whether habitat, diet or sexual selection are primarily responsible for the differences in safety factors observed among species, the cost of producing a relatively larger claw seems an unlikely explanation because safety‐factors did not differ between males and females in any of the sexually dimorphic species.     

Defence Cheats Can Degrade Protection of Chemically Defended Prey

Many species defend themselves against enemies using repellent chemicals. An important but unanswered question is why investment in chemical defence is often variable within prey populations. One explanation is that some prey benefit by cheating, paying no costs of defence, but gaining a reduced attack rate because of the presence of defended conspecifics. Two important assumptions about predator behaviour must be met to explain cheating as a stable strategy: first, predators increase attack rates as cheats increase in frequency; second, defended prey survive attacks better than non‐defended conspecifics. We lack data from wild predators that evaluate these hypotheses. Here, we examine how changes in the frequency of non‐defended ‘cheats’ affect predation by wild birds on a group of otherwise defended prey. We presented mealworm larvae that were either edible (‘cheats’) or unpalatable (bitter tasting), and varied the proportion of cheats from 0 to 1 by increments of 0.25. We found strong frequency‐dependent effects on the birds' foraging behaviour, with the proportion of prey attacked increasing nonlinearly with the frequency of cheats. We did not, however, observe that birds taste‐rejected defended prey at the site of capture. One explanation is that wild birds may not assess prey palatability at the site of capture, but do this elsewhere. If so, defended and undefended prey may pay high costs of initial attack and relocation away from ecologically favourable locations. Alternatively, defended prey may not be taste‐rejected because with acute time constraints, wild birds do not have time to make fine‐grained decisions during feeding. We discuss the data in relation to the evolutionary ecology of prey defences.     

Co‐evolutionary dynamics between public good producers and cheats in the bacterium Pseudomonas aeruginosa

The production of beneficial public goods is common in the microbial world, and so is cheating – the exploitation of public goods by nonproducing mutants. Here, we examine co‐evolutionary dynamics between cooperators and cheats and ask whether cooperators can evolve strategies to reduce the burden of exploitation, and whether cheats in turn can improve their exploitation abilities. We evolved cooperators of the bacterium Pseudomonas aeruginosa, producing the shareable iron‐scavenging siderophore pyoverdine, together with cheats, defective in pyoverdine production but proficient in uptake. We found that cooperators managed to co‐exist with cheats in 56% of all replicates over approximately 150 generations of experimental evolution. Growth and competition assays revealed that co‐existence was fostered by a combination of general adaptions to the media and specific adaptions to the co‐evolving opponent. Phenotypic screening and whole‐genome resequencing of evolved clones confirmed this pattern, and suggest that cooperators became less exploitable by cheats because they significantly reduced their pyoverdine investment. Cheats, meanwhile, improved exploitation efficiency through mutations blocking the costly pyoverdine‐signalling pathway. Moreover, cooperators and cheats evolved reduced motility, a pattern that likely represents adaptation to laboratory conditions, but at the same time also affects social interactions by reducing strain mixing and pyoverdine sharing. Overall, we observed parallel evolution, where co‐existence of cooperators and cheats was enabled by a combination of adaptations to the abiotic and social environment and their interactions.     

Aerodynamic costs of long tails in male barn swallows Hirundo rustica and the evolution of sexual size dimorphism

Exaggerated tail feathers of birds constitute a standard exampleof evolution of extravagant characters due to sexual selection.Such secondary sexual traits are assumed to be costly to produceand maintain, and they usually are accompanied by morphologicaladaptations that tend to reduce their costs. The aerodynamiccosts for male barn swallows Hirundo rustica of having longtails were quantified using aerodynamics theory applied to morphologicaldata from seven European populations. Latitudinal differencesin tail length were positively correlated with differences inflight costs predicted by aerodynamics theory. A positive relationshipbetween aerodynamic costs of long tails and the degree of sexualsize dimorphism was found among populations. Latitudinal differencesin foraging costs may result in tail length being relativelysimilar in males and females in southern populations, whereasthe low foraging costs for males in northern populations mayallow them to cope with higher aerodynamic costs, giving riseto large sexual size dimorphism. Enlargement of wingspan inmales can alleviate but not eliminate the costs of tail exaggeration,and therefore differences in aerodynamic costs of male ornamentswere maintained among populations. Sexual size dimorphism in thebarn swallow arises as a consequence of latitudinal differencesin the advantages of sexual selection for males and the costsof long tails for males and females.     

Harder,better, faster,stronger: Weapon size is more sexually dimorphic than weapon biomechanical components in two freshwater anomuran species

Sexual selection influences the evolution of morphological traits that increase the likelihood of monopolizing scarce resources. When such traits are used during contests, they are termed weapons. Given that resources are typically linked to monopolizing mating partners, theory expects only males to bear weapons. In some species, however, females also bear weapons, although typically smaller than male weapons. Understanding why females bear smaller weapons can thus help us understand the selective pressures behind weapon evolution. However, most of our knowledge comes from studies on weapon size, while the biomechanics of weapons, such as the size of the muscles, efficiency, and shape are seldom studied. Our goal was to test if the theoretical expectations for weapon size sexual dimorphism also occur for weapon biomechanics using two aeglid crab species. Males of both species had larger claws which were also stronger than female claws. Male claws were also more efficient than females' claws (although we used only one species in this analysis). For weapon shape, though, only one species differed in the mean claw shape. Regarding scaling differences, in both species, male claws had higher size scaling than females, while only one species had a higher shape scaling. However, male weapons did not have higher scaling regarding strength and efficiency than females. Thus, males apparently allocate more resources in weapons than females, but once allocated, muscle and efficiency follow a similar developmental pathway in both sexes. Taken together, our results show that sexual dimorphism in weapons involves more than differences in size. Shape differences are especially intriguing because we cannot fully understand its causes. Yet, we highlight that such subtle differences can only be detected by measuring and analysing weapon shape and biomechanical components. Only then we might better understand how weapons are forged.     

Bilateral linkage of monomorphic and dimorphic limb sizes in fiddler crabs

In this study, the subject of whether investment in one bilateral structure was linked to investment in the homologous bilateral opposite structure was investigated. Male fiddler crabs (genus Uca, family Ocypodidae) displayed strong bilateral claw differentiation of function and size, which are used for feeding (minor claw) or display/combat (major claw). Females had similar‐sized feeding claws. Linkage between claw size was investigated by estimating the deviations from an overall fitted regression of claw length to body size. The positive correlations of the deviations of claw size for major and minor claws of males and between right and left claws of females, relative to body size, suggested a linkage in investment between one claw and the corresponding claw on the other side of the body, for both monomorphic females and dimorphic males. A signal to send resources may be effectively gated to the claw complex, suggesting that positively correlated resources are allocated to both claws. Positive correlations were also found at the interspecific level. The fiddler crab model, described here, gives access to study the linkage in symmetric and asymmetric bilateral structures in the same species with a connection to the macroevolutionary level.     

Thermoregulation as an alternate function of the sexually dimorphic fiddler crab claw

Fiddler crabs are highly sexually dimorphic. Males possess one small (minor) feeding claw and one greatly enlarged (major) claw; females possess two small claws. The major claw is used to attract mates and for burrow defense, but it is costly for the male to possess. We tested the hypothesis that the major claw also functions as a thermoregulatory structure, a function that would allow males to spend a greater amount of time at the surface, foraging and attracting potential mates. Fiddler crabs Uca panacea were exposed to a source of radiant heat and body temperatures were monitored. Four groups of crabs were tested: intact males, males with the minor claw removed, males with the major claw removed, and females. The body temperatures of males without the major claw increased more rapidly and reached higher values than did those of males with the major claw intact, but the results from these animals were similar to those of females. These results support the hypothesized thermoregulatory function of the major claw. The major claw may function as a heat sink, transferring heat away from the body and dissipating it into the air. Enhanced thermoregulatory ability provided by the major claw may partially ameliorate the energetic costs of possessing such a large claw.     

Enhanced male coloration after immune challenge increases reproductive potential

In many animal species, females select a mate on the basis of the expression of secondary sexual traits. A prevalent theory suggests that male ornaments are reliable indicators of immunocompetence, because the cost of immune function prevents cheating. However, sexual signalling is a component of male reproductive effort, and an immune challenge may also alter his perceived future prospects and hence signalling effort. In this study, blue‐footed booby males (Sula nebouxii) were inoculated with a diphtheria–tetanus vaccine during courtship to investigate the consequences of mounting an immune response on signalling effort. We found that, after this immune challenge, on average, males increased their signalling effort but lost more body mass compared with control males. Importantly, vaccination affected the partner's reproductive decisions: compared with control females, females paired with vaccinated males laid eggs earlier and increased clutch volume in pairs that laid early. Overall, our results suggest that blue‐footed booby males invest more in sexual signals when future breeding opportunities are at risk, eliciting a greater reproductive investment by their partners. Increased signalling effort by infected individuals may contrast the idea of sexual ornaments as signals of infection status.