Social Monogamy in the Big-Clawed Snapping Shrimp, Alpheus heterochelis

Social monogamy has evolved independently in many taxa, and often involves biparental care of the young. Where it does not, mate guarding and shared territoriality have been invoked as causal factors. We evaluated mate guarding and shared resource defence (a common shelter) as factors that could have led to social monogamy in the snapping shrimp, Alpheus heterochelis. This species is found in male–female pairs that defend a common shelter together. Female receptivity lasts only for a few hours immediately after her periodic moult. Their monogamous pair bond may represent mate guarding or joint defence of a territory. Monogamy in A. heterochelis seems most importantly driven by the cryptic nature of the female's moult cycle. We found that males did not discriminate among females at different intermoult stages for pairing, nor did they modulate their defence of mate and shelter (vs. the risk in finding a new shelter and mate) according to female moult stage. This, together with the short period of female receptivity before her single copulation per cycle, make extended mate guarding the most efficient method for a male to secure a mating opportunity. Comparing eviction rates of paired and unpaired shelter residents by conspecific intruders provided no evidence of enhanced resource defence that would confer a selective advantage to a pair. Male presence during the moult is beneficial for the female, as searching for a male during her soft-bodied receptive phase would put her at mortal risk. Our results show empirically for the first time that guarding may be beneficial, even if males are not able to assess the female's reproductive stage. This extends the theoretical framework for understanding the evolution of social monogamy in taxa without biparental care of young.     

The Round-Eared Sengi and the Evolution of Social Monogamy: Factors that Constrain Males to Live with a Single Female

Animal dispersion in space and time results from environmental pressures, and affects the outcome of a species' social organization. When females are solitary, males may either roam or be pair-living. We studied possible environmental influences affecting the social organization of the round-eared sengi ( Macroscelides proboscideus ) in a semi-desert in South Africa, using trapping and radio-tracking across 2.5 yr. Adult sex ratios did not deviate from 1:1 and we found no indication of sexual dimorphism in body mass. Females maintained exclusive areas, which had little overlap (<4%) with neighbouring females (NF), and males overlapped predominately only with the home range of single females. Generally, inter- and intra-sexual overlap with neighbouring individuals was low (3–6%) for both sexes, indicating territoriality and pair-living. Pairs were perennial and territories were maintained year-round. However, males generally maintained much larger areas than females, which were sensitive to population density. Male space use appeared to be primarily limited by the presence of neighbouring males. Female home ranges were smaller-sized despite changes in population density, possibly for energetic efficiency. Some paired males attempted to take over widowed females, but shifted back to their original home range following the intrusion of an un-paired male. We conclude that social monogamy is the predominant social organization in round-eared sengis in a semi-desert that may have resulted from females living solitarily in small exclusive territories, balanced sex ratios, and from a low variation of body mass between males.     

Integrating Proximate and Ultimate Causation in the Study of Vertebrate Behavior: Methods Considerations

SYNOPSIS. Methods issues are critical for the integration ofproximate and ultimate explanations of animal behavior. Understandingthat evolution of behavior may begin with changes in sensoryand perceptual systems is a first step. For example, advancesin neurobiology can trigger questions about social behavior.Variation in the size of particular brain areas, such as thehippocampus, can be related to variation in socio-spatial systems.Second, procedures, developed in recent years, provide new avenuesto understand behavior. Hormone assay techniques, such as RIAand ELISA, can be performed on some hormones from urine andfeces collected in the wild. Metabolic measurement, such asthe use of doublylabeled water, make it possible to measureenergy costs under field conditions. Advances in DNA technologiesprovide new perspectives, particularly with regard to measuringreproductive success. Third, current theories in behavior canbe tested with regard to physiological mechanisms; all thatis needed is some ingenuity to design and execute appropriatestudies. These include kin recognition, sex ratio variation,and foraging behavior. Fourth, cross—fertilization betweenlaboratory and field approaches produces new insights regardingbehavior. Organizational effects of hormones have now been exploredin field populations of mice and in domestic swine. Testingaspects of foraging behavior in the laboratory is another example.Fifth, simulation models have been used to produce new questionsabout both proximate and ultimate aspects of behavior. Exploringbehavioral phenomena may involve semi—natural settings.The suitability of semi—natural enclosures for the studyof house mouse behavior has been tested with regard to densityand home range size.     

Possible Female Choice During Copulation in Ozophora baranowskii (Heteroptera: Lygaeidae): Female Behavior, Multiple Copulations, and Sperm Transfer

The remarkable behavior of female Ozophora baranowskii of lightly tapping the male with the hind legs during copulation was studied in relation to multiple copulations, copulation length, and sperm transfer. Multiple copulations did not affect female fecundity, fertility, or longevity. The incidence of tapping was higher in shorter copulations, which did not result in sperm transfer to the female. Female tapping behavior may be a mechanism for choosing between males after copulation has begun.     

Sexual Strategy and Size Dimorphism in Rattlesnakes: Integrating Proximate and Ultimate Causation

SYNOPSIS. Integrating proximate and ultimate causes and effectssimultaneously in the study of behavior is challenging and complex,but useful. This is equivalent to asking both "How?" (in thesense of proximate mechanisms) and "Why?" (in the sense of ultimateevolutionary payoffs) an organism operates in one way and notanother. Sex differences in rattlesnake (i) size and growthand (ii) mating and reproductive strategies and tactics, providea good theoretical and empirical context in which to attemptsuch integration. We employ interdisciplinary and multidisciplinaryapproaches in our behavioral and physiological work, but wemean something different by "integrative," that amounts to thesimultaneous study of both proximate and ultimate levels ofcausation and explanation. Though not always feasible, thisapproach represents an important goal to work towards becauseit attempts to represent faithfully the complexity inherentin living systems. To this end, we also employ a variety ofmodeling approaches, which entrain intuition, generate new hypotheses,and sharpen inference. Individual-based simulations, for example,offer promise for broad, integrative programs of biologicalresearch.     

Female parity, male aggression, and the Challenge Hypothesis in wild chimpanzees

The Challenge Hypothesis proposes that testosterone mediates aggression during periods of heightened conflict between males, especially episodes that have important fitness consequences. Considerable evidence from seasonally breeding species provides support for this hypothesis, but few data exist in animals that mate year-round. We tested predictions generated by the Challenge Hypothesis in chimpanzees, a non-seasonally breeding primate, through a study of individuals living in an exceptionally large community at Ngogo, Kibale National Park, Uganda. Results indicated that dominance rank had no influence on testosterone levels. Instead of rank influencing testosterone production, additional analyses revealed an important role for reproductive competition. Male chimpanzees displayed more aggression when they were in the same party as parous estrous females than when reproductively active females were unavailable. Male chimpanzees competed more intensely for mating opportunities with parous females than with nulliparas, and as a consequence, males displayed more aggression around the former than the latter. When males accompanied parous estrous females, their urinary testosterone concentrations were significantly higher than baseline concentrations. In contrast, urinary testosterone concentrations did not exceed baseline when males associated with nulliparous estrous females. These differences in testosterone levels could not be attributed to mating per se because males copulated equally often with parous and nulliparous females. Furthermore, variation in testosterone concentrations were not due to males gathering together in large parties, as their levels in these situations did not exceed baseline. Taken together, these findings, derived from a relatively large sample of males and estrous females, replicate those from a prior study and furnish additional support for the Challenge Hypothesis. Our results suggest that the Challenge Hypothesis is likely to be broadly applicable to chimpanzees and increase our understanding of the physiological costs to males who compete for estrous females.     

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。     

Function and Causation of Social Signals in Lizards

SYNOPSIS. We describe here a multidisciplinary investigationof the stimuli and mechanisms controlling reproduction in thegreen anole lizard, Anolis carolinensis. Bothenvironmental andsocial stimuli that vary seasonally are used as proximate cuesto reproduction. In order for these ecological factors to initiatebreeding, they must be perceived and integrated in the centralnervous system. External and internal stimuli converge uponthe hypothalamus, the major neuroendocrine integrative areaof the brain, which, in turn, directly regulates pituitary andautonomic function. In addition to their role in reproduction,the gonadal hormones are important throughout the life of theorganism, acting both peripherally and centrally, to adapt theindividual to its environment. Thus, the environment, behavior,and physiology interact in complex ways to synchronize the socialand reproductive activities of individuals.     

雌性选择与雄鸟鸣唱的进化

鸣唱是许多鸟类的重要的雄性第二性征之一。雄性鸣唱包含着丰富的信息：物种、领域质量、遗传状态和生理状态。这些信息可被雌性用来判断潜在配偶的素质,而雌性对复杂鸣唱的偏爱反过塑造了鸟类的鸣唱。一般认为雌性选择的调控基因位于决定性别的W染色体上。     

Darwin's Manufactory Hypothesis Is Confirmed and Predicts the Extinction Risk of Extant Birds

In the Origin of Species Darwin hypothesized that the “manufactory” of species operates at different rates in different lineages and that the richness of taxonomic units is autocorrelated across levels of the taxonomic hierarchy. We confirm the manufactory hypothesis using a database of all the world''s extant avian subspecies, species and genera. The hypothesis is confirmed both in correlations across all genera and in paired comparisons controlling for phylogeny. We also find that the modern risk of extinction, as measured by “Red List” classifications, differs across the different categories of genera identified by Darwin. Specifically, species in “manufactory” genera are less likely to be threatened, endangered or recently extinct than are “weak manufactory” genera. Therefore, although Darwin used his hypothesis to investigate past evolutionary processes, we find that the hypothesis also foreshadows future changes to the evolutionary tree.     

Interspecific Differences in the Response of Female Birds to Song Repertoires

The functional significance of the wide variation between bird species in the sizes of individual song repertoires is not understood. We have studied the effects of song repertoires on females. Song triggers copulation solicitation display in female sparrows treated with estradiol. Song sparrow males (Melospiza melodia) have repertoires of about 10 song types, and female song sparrows display significantly more to presentations of large repertoires than to a single song type. By contrast, male field sparrows (Spizella pusilla) and white-throated sparrows (Zonotrichia albicollis) each have only one song type, and their females show no significant increment in responsiveness to repertoires of several song types over a single song type. Swamp sparrows (Melospiza georgiana) fall in between, with male repertoires of three song types. Female swamp sparrows behave in intermediate fashion, responding more to several song types than to one, but the response increment is less than in song sparrows. Thus species differences that males exhibit in song repertoires are paralleled by differences in female responsiveness to multiple song types, implicating variations in female reactivity in the evolution of song repertoires. Female song sparrows respond preferentially to repertoires programmed in eventual variety rather than immediate variety, while field sparrows and white-throated sparrows show no discrimination.     

Maternal Care, Iteroparity and the Evolution of Social Behavior: A Critique of the Semelparity Hypothesis

The Semelparity Hypothesis (Tallamy and Brown in Animal Behav 57:727–730, 1999) predicts that among insects with parental care that iteroparity will be rare. It represents two important challenges. First, life history ecologists have sometimes linked extended parental care with iteroparity, not semelparity, as part of a suite of correlated characters associated with K-selective environments. Second, behavioral ecologists have developed theories for the evolution of eusociality that rely upon a subsocial species producing multiple cohorts of offspring, a precondition for offspring allocare and/or inheritance of a social unit. Using a database of invertebrates exhibiting maternal care in Costa (The other insect societies. Harvard University Press, Cambridge, 2006), the association between semelparity and maternal care was tested using a broad comparative analysis. Semelparity was found in only 24.5 % of the best-studied representative species. In addition, semelparity was more rare in species that form nests, burrows or galleries (12.1 %) than in species that guard offspring out in the open (45.0 %). Iteroparity was common both among nesting species with non-overlapping broods (serial nesting) and in species where a female produces broods of different aged offspring in the same nest (within-nest iteroparity). It is hypothesized that common factors, particularly rapid juvenile development on high quality resources, facilitated both serial nesting and parental care. Within-nest iteroparity is an essential stage in the evolution of eusociality that has often been overlooked. Recent models of sibling conflict and reproductive spacing suggest that parental care can be an indirect cause of within-nest iteroparity despite the fact that parental investment can lead directly to diminished future reproduction. The reversal of this life history correlation may occur as a result of the transition between asocial and subsocial nesting behavior; analogous reversals may be a frequent outcome of transitions between levels of social organization.     

Examining Variation in Recombination Levels in the Human Female: A Test of the Production-Line Hypothesis

The most important risk factor for human aneuploidy is increasing maternal age, but the basis of this association remains unknown. Indeed, one of the earliest models of the maternal-age effect—the “production-line model” proposed by Henderson and Edwards in 1968—remains one of the most-cited explanations. The model has two key components: (1) that the first oocytes to enter meiosis are the first ovulated and (2) that the first to enter meiosis have more recombination events (crossovers) than those that enter meiosis later in fetal life. Studies in rodents have demonstrated that the first oocytes to enter meiosis are indeed the first to be ovulated, but the association between the timing of meiotic entry and recombination levels has not been tested. We recently initiated molecular cytogenetic studies of second-trimester human fetal ovaries, allowing us to directly examine the number and distribution of crossover-associated proteins in prophase-stage oocytes. Our observations on over 8,000 oocytes from 191 ovarian samples demonstrate extraordinary variation in recombination within and among individuals but provide no evidence of a difference in recombination levels between oocytes entering meiosis early in fetal life and those entering late in fetal life. Thus, our data provide a direct test of the second tenet of the production-line model and suggest that it does not provide a plausible explanation for the human maternal-age effect, meaning that—45 years after its introduction—we can finally conclude that the production-line model is not the basis for the maternal-age effect on trisomy.     

Explaining the Paradox of Neophobic Explorers: The Social Information Hypothesis

How animals react to novel food and objects is commonly thought of as a crucial step toward innovations. One would therefore expect innovative species to be attracted to novelty and benefit from a combination of low neophobia and a high motivation to explore. Here we draw attention to the innovation paradox: the most innovative species tend to show neophobic reactions when confronted with novel objects or food, but can use social cues to overcome their initial neophobia. Work on novelty response has highlighted the role of ecological factors as determinants of neophobia and exploration tendency. We examine social influences on novelty response and present the idea that social factors enable some species to maintain the paradoxical combination of high neophobia and high exploration tendency. We compare primates with other species, to assess the extent to which primates are unusual. We review empirical studies that show how intrinsic neophobia is generally overcome by social facilitation and social information, i.e., the presence of experts, especially in species with slow life history, probably because social information reduces risk. We also briefly discuss the role of environmental risk in reducing intrinsic neophobia, in particular its absence in captivity. We draw attention to a strong neophobia-reducing effect of being in captivity, due to humans acting as sources of social information. We propose that species showing the paradoxical combination of strong neophobia and strong exploration tendency use social information to select aspects of the environment worth exploring. The social information hypothesis thus offers an explanation for the paradox of neophobic explorers.     

Forced Copulations and Intra-specific Parasitism: Two Costs of Social Living in the White-fronted Bee-eater

White-fronted bee-eaters are colonially breeding birds that exhibit highly developed helping-at-the-nest. Through long-term studies of an individually-marked population, we have documented two costs of social living: 1) harassment of mated females by extra-pair males, and 2) intra-specific parasitism by females who lay eggs in the nests of others. Breeding females are sexually chased and, occasionally, forceably mated by males other than their mates. Focal-sampling of females throughout their period of receptivity revealed that the average female is involved in 5 to 8 sexual chases and is forceably copulated 0.15 to 0.23 times per breeding season. This risk to females would be much greater were it not for the behavior of male mates who remain close to, and actively defend, their partners. Such mate-guarding is highly effective — females entering and leaving the colony in consort with their mates are sexually harassed only 1/10 as often as females travelling alone. Although sexual harassment of females is common at bee-eater colonies, the risk of paternity uncertainty arising from forced copulations is thought to be low. The reason is that females copulate repeatedly with their male mates on all days immediately prior to as well as during egg laying. This point has been overlooked in previous reports and has led to an exaggeration of the paternity risks associated with forced sexual chases. We conclude that sexual chasing of extra-pair females is a low yield reproductive tactic employed primarily by monogamously mated males whose presence at the colony is required to allofeed and mateguard their own egg-laying females. Female white-fronted bee-eaters lay eggs in nests other than their own. This intraspecific parasitism constitutes a greater threat to certainty of parentage than does forced copulation. Over four years of study, 16% of nests were parasitized and 7 % of all eggs were laid by a female other than the breeder (Table 2). Parasitizing females come primarily from two sources: (1) members of mated pairs whose own breeding attempt is disrupted at the time of egg laying, and (2) single females who opportunistically add an egg at the nest of their parents (or parent plus step-parent). In each case of kin-parasitism, the “parasitic” female remained socially integrated with the host group and helped in the rearing of the young. In contrast, 9 of 10 females that parasitized the nests of non-relatives had no other interactions with the hosts (Table 3). Parasitizing females exhibited two specialized behaviors that enhanced their reproductive effectiveness: (1) they spent many hours observing, investigating, and testing the defenses of potential host nests, and (2) they preferentially laid in hosts' nests at the appropriate chronological stage of development. Breeding females also exhibited counterbehaviors against being parasitized. These included: (1) remaining sequestered in their nest chambers for 64%-65% of the daylight hours and 94 % of the pre-roost hours during their days of egg laying, (2) aggressively defending their nest entrances against all investigating (potentially parasitic) females, and (3) actively removing any eggs laid in their nests prior to the initiation of their own clutch. These tactics and countertactics suggest a long evolutionary history of parasitic opportunities and risks among white-fronted bee-eaters.