Recognition of Dominance in the Big-Clawed Snapping Shrimp ( Alpheus heterochaelis Say 1818) Part II: Analysis of Signal Modality

Alpheus heterochaelis is able to recognise the dominance status of an opponent (see Part I of this series). A former loser does not fight against a former winner but rather escapes immediately after a contact. However, if a former loser meets an inexperienced opponent, the loser fights against it. Here we investigated the signal used for dominance recognition. Two groups of snapping shrimp that had lost a fight on Day 1, intact animals, and shrimp with cut lateral antennular filaments (i.e. without chemosensory aesthetascs), fought against the same winner on Day 2. Intact losers showed escape behaviour, while losers without aesthetascs showed almost the same aggressive behaviour as on Day 1. The main signal in dominance recognition is therefore a chemical one, possibly the urine or a substance carried by it. The main receptor organs for this signal are the lateral filaments of the antennules carrying the aesthetascs.     

Recognition of Dominance in the Big-Clawed Snapping Shrimp (Alpheus heterochaelis Say 1818) Part II: Analysis of Signal Modality

Alpheus heterochaelis is able to recognise the dominance status of an opponent (see Part I of this series). A former loser does not fight against a former winner but rather escapes immediately after a contact. However, if a former loser meets an inexperienced opponent, the loser fights against it. Here we investigated the signal used for dominance recognition. Two groups of snapping shrimp that had lost a fight on Day 1, intact animals, and shrimp with cut lateral antennular filaments (i.e. without chemosensory aesthetascs), fought against the same winner on Day 2. Intact losers showed escape behaviour, while losers without aesthetascs showed almost the same aggressive behaviour as on Day 1. The main signal in dominance recognition is therefore a chemical one, possibly the urine or a substance carried by it. The main receptor organs for this signal are the lateral filaments of the antennules carrying the aesthetascs.     

Individual discrimination in the big-clawed snapping shrimp,Alpheus heterochelis

Rahman et al. (Rahman, N., Dunham, D.W. and Govind, C.K. (). Mate recognition and pairing in the big-clawed snapping shrimp, Alpheus herterochelis. Mar. Fresh. Behav. Physiol., 34, 213–226.) demonstrated discrimination by snapping shrimp between former mates and unfamiliar conspecifics, but did not test individual discrimination. In the present study, snapping shrimp showed discrimination between familiar and unfamiliar same-sex conspecifics by preferentially entering that arm of a Y-maze leading to familiar individuals. Furthermore, after being exposed to water from the home tanks of unknown individuals, they later showed an elevated response to this water, if the direction from which the water came into their tank was changed to be novel. This indicates that test subjects associated a familiar chemical stimulus with its location in the environment. This discrimination could only have been made if that chemical signature were recognised as different from that of another chemically familiar individual. This result also demonstrates that the water surrounding an individual contains sufficient (chemical) information to allow discrimination of one individual from another.     

Individual discrimination in the big-clawed snapping shrimp, Alpheus heterochelis

Rahman et al. (Rahman, N., Dunham, D.W. and Govind, C.K. (2001). Mate recognition and pairing in the big-clawed snapping shrimp, Alpheus herterochelis. Mar. Fresh. Behav. Physiol., 34, 213-226.) demonstrated discrimination by snapping shrimp between former mates and unfamiliar conspecifics, but did not test individual discrimination. In the present study, snapping shrimp showed discrimination between familiar and unfamiliar same-sex conspecifics by preferentially entering that arm of a Y-maze leading to familiar individuals. Furthermore, after being exposed to water from the home tanks of unknown individuals, they later showed an elevated response to this water, if the direction from which the water came into their tank was changed to be novel. This indicates that test subjects associated a familiar chemical stimulus with its location in the environment. This discrimination could only have been made if that chemical signature were recognised as different from that of another chemically familiar individual. This result also demonstrates that the water surrounding an individual contains sufficient (chemical) information to allow discrimination of one individual from another.     

Monogamy in a Hyper-Symbiotic Shrimp

Theory predicts that monogamy is adaptive in resource-specialist symbiotic crustaceans inhabiting relatively small and morphologically simple hosts in tropical environments where predation risk away from hosts is high. We tested this prediction in Pontonia manningi, a hyper-symbiotic shrimp that dwells in the mantle cavity of the Atlantic winged oyster Pteria colymbus that, in turn, infects gorgonians from the genus Pseudopterogorgia in the Caribbean Sea. In agreement with theory, P. manningi were found dwelling as heterosexual pairs in oysters more frequently than expected by chance alone. Males and females also inhabited the same host individual independent of the female gravid condition or of the developmental stage of brooded embryos. While the observations above argue in favor of monogamy in P. manningi, there is evidence to suggest that males of the studied species are moderately promiscuous. That females found living solitary in oysters most often brooded embryos, and that males allocated more to weaponry (major claw size) than females at any given size suggest that males might be roaming among host individuals in search of and, fighting for, receptive females. All available information depicts a rather complex mating system in P. manningi: primarily monogamous but with moderately promiscuous males.     

Changes in myofibrillar gene expression during fiber-type transformation in the claw closer muscles of the snapping shrimp, Alpheus heterochelis

Isotopes of a number of crustacean myofibrillar proteins have been identified with sodium dodecyl sulfate-polyacrylamide electrophoresis, and their distribution in muscles of the snapping shrimp has been examined. Fast-slow differences in distribution have been observed for myosin light chains and tropomyosin. In contrast, three troponin T subunits have been resolved, each specific to one of the three muscles examined. This result suggests that expression of crustacean contractile proteins is not accomplished by a simple coexpression of a battery of slow or fast isotopes. In addition, the expression of these proteins was examined during the quasi-developmental fiber-type transition of the main claw closer muscle during the reversal of claw asymmetry in response to the loss of the large snapper appendage. The changes observed appear similar to the cross-innervation induced changes in gene expression of vertebrate muscle.     

Snapping behaviour in intraspecific agonistic encounters in the snapping shrimp (Alpheus heterochaelis)

During intraspecific agonistic encounters in snapping shrimp (Alpheus heterochaelis) the behaviour of the snapper, emitting a fast water jet by very rapid closure of the large modified snapper claw, and the receiver was analysed by single frame video analysis before, during, and after the snap. During snapping the opponents usually face each other. Snapping is most frequently preceded by touch of frontal appendages. The snapping animal keeps its snapper claw slightly across the midline, shielding frontal body parts, and its tailfan bent downwards. The mean claw cocking duration (generating muscle tension) before snapping amounts to about 500 ms. In 58% of the snaps, the snapper claw pointed at the opponent, its claws, densely covered with sensory hairs, representing the main target of the water jet. The mean distance for these directed snaps was 0.9 cm, while undirected snaps were emitted from larger distances of on average 3.4 cm. The snapper usually withdraws immediately after snapping, the receiver approaches. Initial snaps are often answered by return snaps and both are emitted from smaller distances and hit more often than subsequent snaps.     

A comparative study by serial electron microscopy of neuromuscular junctions in the dimorphic claws of the snapping shrimp, Alpheus heterochelis

We compared the neuromuscular junctions on the main closer muscle in the first pair of chelipeds in the snapping shrimp Alpheus heterochelis by serial section electron microscopy. We sought an ultrastructural basis for the different behavioral and physiological functions of these dimorphic claws and for the role of the nervous system in claw transformation. We were unable to detect any statistically significant morphological differences between the junctions. Further, we found the muscle fiber populations and filament arrangements, as well as the electrical properties of the fibers, to be more homogeneous and similar to each other in A. heterochelis than those reported for another species, A. armillatus. We consider our results in light of recent data on the anatomy and electrical properties of the motor neurons within the CNS and conclude that the neural trigger for claw transformation involves factors not revealed by conventional electron microscopy.     

Vortex Formation with a Snapping Shrimp Claw

Snapping shrimp use one oversized claw to generate a cavitating high speed water jet for hunting, defence and communication. This work is an experimental investigation about the jet generation. Snapping shrimp (Alpheus-bellulus) were investigated by using an enlarged transparent model reproducing the closure of the snapper claw. Flow inside the model was studied using both High-Speed Particle Image Velocimetry (HS-PIV) and flow visualization. During claw closure a channel-like cavity was formed between the plunger and the socket featuring a nozzle-type contour at the orifice. Closing the mechanism led to the formation of a leading vortex ring with a dimensionless formation number of approximate ΔT*≈4. This indicates that the claw might work at maximum efficiency, i.e. maximum vortex strength was achieved by a minimum of fluid volume ejected. The subsequent vortex cavitation with the formation of an axial reentrant jet is a reasonable explanation for the large penetration depth of the water jet. That snapping shrimp can reach with their claw-induced flow. Within such a cavitation process, an axial reentrant jet is generated in the hollow cylindrical core of the cavitated vortex that pushes the front further downstream and whose length can exceed the initial jet penetration depth by several times.     

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.     

The Curious Acoustic Behavior of Estuarine Snapping Shrimp: Temporal Patterns of Snapping Shrimp Sound in Sub-Tidal Oyster Reef Habitat

Ocean soundscapes convey important sensory information to marine life. Like many mid-to-low latitude coastal areas worldwide, the high-frequency (>1.5 kHz) soundscape of oyster reef habitat within the West Bay Marine Reserve (36°N, 76°W) is dominated by the impulsive, short-duration signals generated by snapping shrimp. Between June 2011 and July 2012, a single hydrophone deployed within West Bay was programmed to record 60 or 30 seconds of acoustic data every 15 or 30 minutes. Envelope correlation and amplitude information were then used to count shrimp snaps within these recordings. The observed snap rates vary from 1500–2000 snaps per minute during summer to <100 snaps per minute during winter. Sound pressure levels are positively correlated with snap rate (r = 0.71–0.92) and vary seasonally by ~15 decibels in the 1.5–20 kHz range. Snap rates are positively correlated with water temperatures (r = 0.81–0.93), as well as potentially influenced by climate-driven changes in water quality. Light availability modulates snap rate on diurnal time scales, with most days exhibiting a significant preference for either nighttime or daytime snapping, and many showing additional crepuscular increases. During mid-summer, the number of snaps occurring at night is 5–10% more than predicted by a random model; however, this pattern is reversed between August and April, with an excess of up to 25% more snaps recorded during the day in the mid-winter. Diurnal variability in sound pressure levels is largest in the mid-winter, when the overall rate of snapping is at its lowest, and the percentage difference between daytime and nighttime activity is at its highest. This work highlights our lack of knowledge regarding the ecology and acoustic behavior of one of the most dominant soniforous invertebrate species in coastal systems. It also underscores the necessity of long-duration, high-temporal-resolution sampling in efforts to understand the bioacoustics of animal behaviors and associated changes within the marine soundscape.     

Parallel Saltational Evolution of Ultrafast Movements in Snapping Shrimp Claws

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Sex and Weapons: Contrasting Sexual Dimorphisms in Weaponry and Aggression in Snapping Shrimp

Sexual dimorphisms in weaponry and aggression are common in species in which one sex (usually males) competes for access to mates or resources necessary for reproduction – sexually dimorphic weaponry and aggression, in other words, are frequently the result of intrasexual selection. In snapping shrimp, the major chela (snapping claw) can be a deadly weapon, and males of many species have larger chelae than females, a pattern readily interpreted as resulting from intrasexual selection. Thus, males might be expected to show more sex‐specific aggression than females, and be more aggressive overall. We tested these predictions in two species of snapping shrimp in a territorial defense context. Neither of these predictions was supported: in both species, females, but not males, engaged in sex‐specific aggression and females were more aggressive than males overall. These contrasting sexual dimorphisms – larger weaponry in males but higher aggression in females – highlight the importance of considering the function of weaponry and aggression in contexts other than direct competitions over mates. In addition, species differences in the degree of sexual dimorphism in chela size were due to differences in female, not male, chela size, and the species with greater sexual dimorphism in weaponry was significantly less aggressive overall; also, while paired and solitary males did not differ in residual chela size, for the species with greater sexual dimorphism, females carrying embryos had smaller residual chela sizes. These results suggest that understanding the sexual dimorphisms in weaponry and aggression in snapping shrimp requires understanding the relative costs and benefits of both in females as well as males.     

Monogamy in lizards

Monogamy is relatively rarely reported in taxa other than birds. The reproductive system of many lizard species appears to involve multiple mating partners for both the male and the female. However, short-term monogamous relationships have been reported in some lizard species, either where the male defends a territory that is only occupied by a single adult female, or where males stay with females for a period of time after mating, apparently to guard against rival males. There are a few reported cases of more prolonged monogamous relationships in lizards, with the Australian sleepy lizard, Tiliqua rugosa, the best studied example. Adult males and females of this species form monogamous pairs for an extended period before mating each spring, and they select the same partner in successive years. The paper reviews possible functions of monogamy in this and other lizard species, and suggests that the additional perspective from studying lizards may enrich our overall understanding of monogamous behaviour.     

Ultimate Causation of Aggressive and Forced Copulation in Birds: Female Resistance, the CODE Hypothesis, and Social Monogamy

SYNOPSIS. Except in ducks and geese (Anseriforms), aggressiveor forced copulation in birds is rare. The rarity of forcedcopulation in birds theoretically is dueto morphological andphysiological mechanisms of female resistance that place fertilizationmost often under female control. Traits theoretically associatedwith resistance by females include: digestive epithelium liningthe section of the cloaca receiving sperm and powerful doacalmusculature used to eject contents, including waste materialand sperm. These traits suggest that the Immediate FertilizationEnhancement Hypothesis may be an inadequate ultimate explanationfor forced copulation when it occurs. Ideas in Heinroth (1911)and Brownmiller (1975) suggested an alternative, the CODE Hypothesis,which says that aggressive copulation creates a dangerous environmentfor females. This, in turn, fosters male mating advantage viasocial monogamy, because selection sometimes favors femaleswho trade sexual and social access for protection from maleaggression. Thus, theoretically, "trades" of protection forcopulation favor the evolution of social monogamy even in specieswith little or no paternal care. Individual males may accrueselective advantages through direct benefits, kin-selected benefits,or reciprocal altruism. The CODE hypothesis for social monogamypredicts variation in extrapair paternity from preferred mates,variation in male reproductive success, and variation amongfemales' post-insemination resistance mechanisms as functionsof variation among females' vulnerabilities (ecological andintrinsic) to aggressive copulation. Observers will base intraspecifictests on variation among females in their vulnerabilities tomale aggression against them.     

Monogamy in marine fishes

The formation of long-term pair bonds in marine fish has elicited much empirical study. However, the evolutionary mechanisms involved remain contested and previous theoretical frameworks developed to explain monogamy in birds and mammals are not applicable to many cases of monogamy in marine fish. In this review, we summarise all reported occurrences of social monogamy in marine fish, which has so far been observed in 18 fish families. We test quantitatively the role of ecological and behavioural traits previously suggested to be important for the evolution of monogamy and show that monogamous species occur primarily in the tropics and are associated with coral reef environments in which territory defence and site attachment is facilitated. However, there is little evidence that obligately monogamous species are smaller in body size than species that can adopt a polygynous mating system. We review the evidence pertaining to six hypotheses suggested for the evolution of monogamous pair bonds: (1) biparental care, (2) habitat limitation, (3) low population density/low mate availability/low mobility, (4) increased reproductive efficiency, (5) territory defence, and (6) net benefit of single mate sequestration. We outline predictions and associated empirical tests that can distinguish between these hypotheses, and assess how generally each hypothesis explains monogamy within and between breeding periods for species with different types of territories (i.e. feeding only or feeding and breeding). Hypotheses (1) and (2) have limited applicability to marine fishes, while hypotheses (3)-(5) have little empirical support beyond the species for which they were designed. However, the role of paternal care in promoting monogamous pair bonds is not explicit in these hypotheses, yet paternal care has been reported in more than 70 monogamous marine fish. We show that paternal care may act to increase the likelihood of monogamy in combination with each of the proposed hypotheses through decreased benefits to males from searching for additional mates or increased advantages to females from sequestering a single high-quality mate. Among species defending breeding and feeding territories, the benefits, both within and between reproductive periods, of sequestering a single high-quality mate (hypothesis 6) appear to be the best explanation for socially monogamous pairs. For species without parental care (i.e. holding only feeding territories), territory defence (hypothesis 5) in combination with the benefits of guarding a large mate (hypothesis 6) could potentially explain most instances of monogamy. Empirical studies of marine fishes over the past two decades are therefore slowly changing the view of monogamy from a mating system imposed upon species by environmental constraints to one with direct benefits to both sexes.     

小型田鼠:研究单配制进化与调控的模型

哺乳动物的单配制通常被认为是社会性单配制,它不是单纯地由性行为来决定,而是由诸多因素,包括长期的pair bond、夫妻双方共同抚育后代、免近亲交配以及雌雄两性相似等来决定的。在这篇综述中,我们论述了如何以啮齿类田鼠属(Microtus)为模型,通过比较研究来帮助我们理解社会性单配制的进化以及其神经调控机制。对田鼠属的研究不仅证实了单配制起源于艰苦的生存条件的假说,而且还证实了雌性性选择可能有利于维持单配制。不仅如此,哺乳动物单配制的进化还需要雄性的prosocial行为的不断强化。例如,亲近行为可以促进pairbond的形成并强化雄性对后代的哺育行为,而这种强化则来源于神经多肽催产素(OT)和加压素(AVP)与类固醇类激素的相互作用。催产素和加压素调控pairbond和双亲哺育行为的表达,而单配制和多配制田鼠的催产素和加压素受体在脑内的分布有显的不同。比较研究揭示了小型田鼠单配制的调控机制,而种内差异和行为上的可塑性则有助于我们进一步理解这种机制。比如,在某些条件下,多配制的草原田鼠(Microtus pennsylvanicu)的雄性个体具有哺育后代的行为。尽管草原田鼠的加压素Vla受体在脑内的分布与其他多配制的田鼠相似,但是如果脑室注射加压素,仍可以诱发其哺育后代的行为。同样是单配制的橙腹田鼠(Microtus ochrogaster),生活在：Illnois的显示出高水平的prosocial行为,而生活在Kansas的则表现出较低水平的社会性行为。即使两个种群的催产素或加压素Vla受体在脑内的分布相同,它们的雌激素受体表达水平显不同,这在雄性个体表现尤其明显。与Kansas的雄性个体相比,在终纹床核(bed rucleus of the stria tenninalis)和杏仁核中区(medial amygdala)这两个调控亲近行为和攻击行为的脑区,Illinois的雄性个体的α雌激素受体的水平要低得多。这些研究表明对雌激素的低敏感程度有利于高水平地表达prosocial行为并降低特定类型的攻击行为。     

Monogamy,strongly bonded groups,and the evolution of human social structure

Human social evolution has most often been treated in a piecemeal fashion, with studies focusing on the evolution of specific components of human society such as pair‐bonding, cooperative hunting, male provisioning, grandmothering, cooperative breeding, food sharing, male competition, male violence, sexual coercion, territoriality, and between‐group conflicts. Evolutionary models about any one of those components are usually concerned with two categories of questions, one relating to the origins of the component and the other to its impact on the evolution of human cognition and social life. Remarkably few studies have been concerned with the evolution of the entity that integrates all components, the human social system itself. That social system has as its core feature human social structure, which I define here as the common denominator of all human societies in terms of group composition, mating system, residence patterns, and kinship structures. The paucity of information on the evolution of human social structure poses substantial problems because that information is useful, if not essential, to assess both the origins and impact of any particular aspect of human society.