Social regulation of reproduction: control or signal?

Traditionally, dominant breeders have been considered to be able to control the reproduction of other individuals in multimember groups that have high variance in reproductive success/reproductive skew (e.g., forced sterility/coercion of conspecifics in eusocial animals; sex-change suppression in sequential hermaphrodites). These actions are typically presented as active impositions by reproductively dominant individuals. However, how can individuals regulate the reproductive physiology of others? Alternatively, all contestants make reproductive decisions, and less successful individuals self-downregulate reproduction in the presence of dominant breeders. Shifting perspective from a top-down manipulation to a broader view, which includes all contenders, and using a multitaxon approach, we propose a unifying framework for the resolution of reproductive skew conflicts based on signalling rather than control, along a continuum of levels of strategic regulation of reproduction.

The oxidative cost of competing for egg fertilization exceeds the cost of egg production.

Measuring reproductive costs is crucial to understanding sexual conflict and its evolutionary outcomes. Sexual conflict is thought to originate from anisogamy-the size difference between male and female gametes; if sperm are tiny and not produced in vastly greater numbers than eggs, at any mating females' gametic investment is larger than that of males. Testing this prediction has proven difficult, especially because males and females differ in many more traits than just gamete size. We overcame this difficulty by exposing simultaneously hermaphroditic polychaete worms Ophryotrocha diadema (two sexual functions in the same body) to two social conditions, pairs, and groups >2, where hermaphrodites invest either relatively more in the female function or relatively more in the male function, respectively. Then we measured four markers of cellular oxidative status, a physiological mediator of life-history strategies. Less female-biased hermaphrodites produced fewer eggs but, unexpectedly, had lower levels of antioxidant protection than more female-biased hermaphrodites, which produced more eggs. Male-biased hermaphrodites compete for mating as males (hermaphrodites in pairs do not) suggesting that in the short-term male competition might be costlier than egg production in terms of regulation of oxidative status. These results highlight the need of including behavioral traits, namely competition over egg fertilization, in the measures of reproductive costs.

Genome and cuticular hydrocarbon-based species delimitation shed light on potential drivers of speciation in a Neotropical ant species complex.

Geographic separation that leads to the evolution of reproductive isolation between populations generally is considered the most common form of speciation. However, speciation may also occur in the absence of geographic barriers due to phenotypic and genotypic factors such as chemical cue divergence, mating signal divergence, and mitonuclear conflict. Here, we performed an integrative study based on two genome-wide techniques (3RAD and ultraconserved elements) coupled with cuticular hydrocarbon (CHC) and mitochondrial (mt) DNA sequence data, to assess the species limits within the Ectatomma ruidum species complex, a widespread and conspicuous group of Neotropical ants for which heteroplasmy (i.e., presence of multiple mtDNA variants in an individual) has been recently discovered in some populations from southeast Mexico. Our analyses indicate the existence of at least five distinct species in this complex: two widely distributed across the Neotropics, and three that are restricted to southeast Mexico and that apparently have high levels of heteroplasmy. We found that species boundaries in the complex did not coincide with geographic barriers. We therefore consider possible roles of alternative drivers that may have promoted the observed patterns of speciation, including mitonuclear incompatibility, CHC differentiation, and colony structure. Our study highlights the importance of simultaneously assessing different sources of evidence to disentangle the species limits of taxa with complicated evolutionary histories.

Chemically Insignificant Social Parasites Exhibit More Anti-Dehydration Behaviors than Their Hosts.

Social parasites have evolved adaptations to overcome host resistance as they infiltrate host colonies and establish there. Among the chemical adaptations, a few species are chemically "insignificant"; they are poor in recognition cues (cuticular hydrocarbons) and evade host detection. As cuticular hydrocarbons also serve a waterproofing function, chemical insignificance is beneficial as it protects parasites from being detected but is potentially harmful because it exposes parasites to desiccation stress. Here I tested whether the social parasites Polistes atrimandibularis employ behavioral water-saving strategies when they live at Polistes biglumis colonies. Observations in the field showed that parasites were less active than their cohabiting host foundresses, spent more time at the nest, and rested in the shadowy, back face of the nest, rather than at the front face, which contradicted expectations for the use of space for dominant females-typically, dominants rest at the nest front-face. These data suggest that behavioral adaptations might promote resistance to desiccation stress in chemical insignificant social parasites.

Egg-trading worms start reciprocation with caution, respond with confidence and care about partners' quality.

Conditional reciprocity (help someone who helped you before) explains the evolution of cooperation among unrelated individuals who take turns helping each other. Reciprocity is vulnerable to exploitations, and players are expected to identify uncooperative partners who do not return the help they received. We tested this prediction in the simultaneously hermaphroditic worm, Ophryotrocha diadema, which engages in mutual egg donations by alternating sexual roles (one worm releases' eggs and the other fertilizes them). We set up dyads with different cooperativeness expectations; partners were either the same or a different body size (body size predicts clutch size). Large worms offered larger clutches and did so sooner when paired with large rather than small partners. They also released smaller egg clutches when they started egg donations than when they responded to a partners' donation, fulfilling the prediction that a players' first move will be prudent. Finally, behavioral bodily interactions were more frequent between more size-dissimilar worms, suggesting that worms engaged in low-cost behavioral exchanges before investing in such costly moves as egg donations. These results support the hypothesis that simultaneously hermaphroditic worms follow a conditional reciprocity paradigm and solve the conflict over sexual roles by sharing the costs of reproduction via the male and the female functions.

A Stresipteran parasite extends the lifespan of workers in a social wasp.

In social wasps, female lifespan depends on caste and colony tasks: workers usually live a few weeks while queens as long as 1 year. Polistes dominula paper wasps infected by the strepsipteran parasite Xenos vesparum avoid all colony tasks, cluster on vegetation where parasite dispersal and mating occur, hibernate and infect the next generation of wasp larvae. Here, we compared the survival rate of infected and uninfected wasp workers. Workers' survival was significantly affected by parasite sex: two-third of workers parasitized by a X. vesparum female survived and overwintered like future queens did, while all workers infected by a X. vesparum male died during the summer, like uninfected workers that we used as controls. We measured a set of host and parasite traits possibly associated with the observed lifespan extension. Infected overwintering workers had larger fat bodies than infected workers that died in the summer, but they had similar body size and ovary development. Furthermore, we recorded a positive correlation between parasite and host body sizes. We hypothesize that the manipulation of worker's longevity operated by X. vesparum enhances parasite's fitness: if workers infected by a female overwinter, they can spread infective parasite larvae in the spring like parasitized gynes do, thus contributing to parasite transmission.

Strong Gene Flow Undermines Local Adaptations in a Host Parasite System.

The co-evolutionary pathways followed by hosts and parasites strongly depend on the adaptive potential of antagonists and its underlying genetic architecture. Geographically structured populations of interacting species often experience local differences in the strength of reciprocal selection pressures, which can result in a geographic mosaic of co-evolution. One example of such a system is the boreo-montane social wasp Polistes biglumis and its social parasite Polistes atrimandibularis, which have evolved local defense and counter-defense mechanisms to match their antagonist. In this work, we study spatial genetic structure of P. biglumis and P. atrimandibularis populations at local and regional scales in the Alps, by using nuclear markers (DNA microsatellites, AFLP) and mitochondrial sequences. Both the host and the parasite populations harbored similar amounts of genetic variation. Host populations were not genetically structured at the local scale, but geographic regions were significantly differentiated from each other in both the host and the parasite in all markers. The net dispersal inferred from genetic differentiation was similar in the host and the parasite, which may be due to the annual migration pattern of the parasites between alpine and lowland populations. Thus, the apparent dispersal barriers (i.e., high mountains) do not restrict gene flow as expected and there are no important gene flow differences between the species, which contradict the hypothesis that restricted gene flow is required for local adaptations to evolve.

Quantitative Matching of Clutch Size in Reciprocating Hermaphroditic Worms.

Reciprocity [1] is one of the most controversial evolutionary explanations of cooperation among non-kin [2, 3]. For some authors, cognitive capacity of non-human organisms is limiting, and more parsimonious mechanisms should apply [3-5]; for others, the debate is mainly semantic [2, 6], and empirical evidence can be found in a wide range of taxa [7]. However, while the ability to alternate cooperative behaviors does not settle the reciprocity controversy, the capacity to adjust cooperative behavior to the value of received help could prove decisive. Marine polychaete worms Ophryotrocha diadema, as several simultaneous hermaphrodites, do not self-fertilize and have unilateral mating (i.e., they behave either as females or as males during each mating event). They are also external fertilizers and thus cannot store allosperm, which contribute to make them ideal model organisms to investigate reciprocity, since partners usually alternate sexual roles with each other, repeatedly exchanging egg clutch of variable size [8-12]. However, whether the alternation of sexual roles is the result of conditional reciprocity rather than by-product reciprocity has never been tested [13]. Here, we show that O. diadema worms reciprocate eggs conditionally to the partner's behavior and adjust the quality of cooperation according to that of their partners. Moreover, only egg reciprocation offers similar fitness returns via both the female and the male function with respect to non-reciprocating laying strategies. These results document that fine-tuned forms of conditional reciprocity can emerge in cognitively unsophisticated animals, broadening the criteria to recognize conditional reciprocity among animals.

Nest signature changes throughout colony cycle and after social parasite invasion in social wasps.

Social insects recognize their nestmates by means of a cuticular hydrocarbon signature shared by colony members, but how nest signature changes across time has been rarely tested in longitudinal studies and in the field. In social wasps, the chemical signature is also deposited on the nest surface, where it is used by newly emerged wasps as a reference to learn their colony odor. Here, we investigate the temporal variations of the chemical signature that wasps have deposited on their nests. We followed the fate of the colonies of the social paper wasp Polistes biglumis in their natural environment from colony foundation to decline. Because some colonies were invaded by the social parasite Polistes atrimandibularis, we also tested the effects of social parasites on the nest signature. We observed that, as the season progresses, the nest signature changed; the overall abundance of hydrocarbons as well as the proportion of longer-chain and branched hydrocarbons increased. Where present, social parasites altered the host-nest signature qualitatively (adding parasite-specific alkenes) and quantitatively (by interfering with the increase in overall hydrocarbon abundance). Our results show that 1) colony odor is highly dynamic both in colonies controlled by legitimate foundresses and in those controlled by social parasites; 2) emerged offspring contribute little to colony signature, if at all, in comparison to foundresses; and 3) social parasites, that later mimic host signature, initially mark host nests with species-specific hydrocarbons. This study implies that important updating of the neural template used in nestmate recognition should occur in social insects.

Population diversity in cuticular hydrocarbons and mtDNA in a mountain social wasp.

Nestmate recognition is a common phenomenon in social insects that typically is mediated by cuticular hydrocarbons. Geographical variation in cuticular hydrocarbons has been observed, although the pattern of variation is not consistent across species and is usually related to the biology and ecology of the different species. Polistes biglumis (Hymenoptera: Vespidae) is a social wasp that lives in high mountains where populations are separated by significant geographical barriers. Here we investigated the level of chemical variation among populations of P. biglumis in the Alps, and shed light on the phylogeography of this species. Populations could be discriminated by means of their cuticular hydrocarbon profiles, which showed a pattern consistent with the isolation-by-distance hypothesis. Molecular data highlighted two areas with different levels of haplotype diversity, although all wasps belonged to the same species. These results suggest that the populations of P. biglumis in the Alps are geographically isolated from one another, favoring their genetic and chemical differentiation.

Early social conditions affect female fecundity in hermaphrodites.

Social conditions experienced prior to sexual maturity influence reproduction later in life in many animals. In simultaneous hermaphrodites, variation in mating group size influences reproductive investment. As the mating group size increases, reproductive resources devoted to the female function decrease in favor of the male function. Prior to sexual maturity, many hermaphrodites have a protandrous phase during which they produce sperm and can fertilize hermaphrodites' eggs. In the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema, the cost of male reproduction during adolescence is spread over the whole energy budget of worms as shown by a reduced growth rate, a delayed age at sexual maturity and the shortening of life span compared to protandrous males that do not reproduce. Little is known on whether social conditions experienced during development affect reproductive investment of immature individuals. We investigated whether social conditions affected the length of the protandrous phase, body size and also the subsequent female fecundity of same-age protandrous individuals of O. diadema, which did not had to face competition for egg fertilization. Results show that in large group sizes protandrous males lengthened their protandrous phase, slowed down body growth and decreased their individual investment at the first egg laying compared to protandrous males that were reared in isolation. In the successive egg layings worms adjusted their egg output to the current social conditions. We interpreted these results as an indication that early social conditions represent a social stress resulting in a reduction of the overall reproductive resources up to the first egg laying.

Changes in the hydrocarbon proportions of colony odor and their consequences on nestmate recognition in social wasps.

In social insects, colonies have exclusive memberships and residents promptly detect and reject non-nestmates. Blends of epicuticular hydrocarbons communicate colony affiliation, but the question remains how social insects use the complex information in the blends to discriminate between nestmates and non-nestmates. To test this we altered colony odor by simulating interspecific nest usurpation. We split Polistes dominulus paper-wasp nests into two halves and assigned a half to the original foundress and the other half to a P. nimphus usurper for 4 days. We then removed foundresses and usurpers from nests and investigated whether emerging P. dominulus workers recognized their never-before-encountered mothers, usurpers and non-nestmates of the two species. Behavioral and chemical analyses of wasps and nests indicated that 1) foundresses marked their nests with their cuticular hydrocarbons; 2) usurpers overmarked foundress marks and 3) emerging workers learned colony odor from nests as the odor of the female that was last on nest. However, notwithstanding colony odor was usurper-biased in usurped nests, workers from these nests recognized their mothers, suggesting that there were pre-imaginal and/or genetically encoded components in colony-odor learning. Surprisingly, workers from usurped nests also erroneously tolerated P. nimphus non-nestmates, suggesting they could not tell odor differences between their P. nimphus usurpers and P. nimphus non-nestmates. Usurpers changed the odors of their nests quantitatively, because the two species had cuticular hydrocarbon profiles that differed only quantitatively. Possibly, P. dominulus workers were unable to detect differences between nestmate and non-nestmate P. nimphus because the concentration of some peaks in these wasps was beyond the range of workers' discriminatory abilities (as stated by Weber's law). Indeed, workers displayed the least discrimination abilities in the usurped nests where the relative odor changes due to usurpation were the largest, suggesting that hydrocarbon variations beyond species-specific ranges can alter discrimination abilities.

Cleptoparasites, social parasites and a common host: chemical insignificance for visiting host nests, chemical mimicry for living in.

Social insect colonies contain attractive resources for many organisms. Cleptoparasites sneak into their nests and steal food resources. Social parasites sneak into their social organisations and exploit them for reproduction. Both cleptoparasites and social parasites overcome the ability of social insects to detect intruders, which is mainly based on chemoreception. Here we compared the chemical strategies of social parasites and cleptoparasites that target the same host and analyse the implication of the results for the understanding of nestmate recognition mechanisms. The social parasitic wasp Polistes atrimandibularis (Hymenoptera: Vespidae), and the cleptoparasitic velvet ant Mutilla europaea (Hymenoptera: Mutillidae), both target the colonies of the paper wasp Polistes biglumis (Hymenoptera: Vespidae). There is no chemical mimicry with hosts in the cuticular chemical profiles of velvet ants and pre-invasion social parasites, but both have lower concentrations of recognition cues (chemical insignificance) and lower proportions of branched alkanes than their hosts. Additionally, they both have larger proportions of alkenes than their hosts. In contrast, post-invasion obligate social parasites have proportions of branched hydrocarbons as large as those of their hosts and their overall cuticular profiles resemble those of their hosts. These results suggest that the chemical strategies for evading host detection vary according to the lifestyles of the parasites. Cleptoparasites and pre-invasion social parasites that sneak into host colonies limit host overaggression by having few recognition cues, whereas post-invasion social parasites that sneak into their host social structure facilitate social integration by chemical mimicry with colony members.

Effects of respiratory therapist-directed protocol on prescription and outcomes of pulmonary rehabilitation in COPD inpatients.

BACKGROUND: The use of respiratory therapist-directed (RD) protocols in non-ICU hospitalized patients decreases respiratory care charges as compared with physician-directed (PD) protocols. OBJECTIVES: To determine whether RD or PD protocol assessments in COPD patients may impact: (1) prescription of respiratory treatments, and (2) outcomes of pulmonary rehabilitation program (PRP). METHODS: In a retrospective observational case-control study, 73 cases (RD) were compared with controls (PD) matched for age, sex, FEV1 and diagnosis of either chronic airflow obstruction (CAO), pulmonary emphysema (PE) or chronic respiratory insufficiency (CRI). PRP programs were specifically tailored and assessed for inpatients with moderate to severe COPD. Type of PRP protocol (P), number of respiratory treatments (RT), number of exercise training prescription (EXP) and failure (EXF), time to start PRP (T) and length of hospital stay (LOS) were recorded. Perceived breathlessness (B) as assessed by MRC scale, 6-min walk meters (6MWD), and BORG-dyspnea at rest (D-rest) and end of effort (D-effort) were also assessed as outcome measures before (T0) and after (T1) the PRP. RESULTS: Frequency distribution of P, EXP and EXF was similar in the two groups. However, prescription of additional RT (1.9 +/- 0.8 and 2.5 +/- 1.1 days, p<0.01), T (1.2 +/- 0.4 and 1.8 +/- 1.2 days, p<0.001) and LOS (17.2 +/- 2.0 and 18.2 +/- 1.8 days, p<0.05) were lower in cases than in controls. Both cases and controls similarly improved (p<0.0001) B, 6MWD, D-rest and D-effort at T1. CONCLUSIONS: RT-directed assessment results in less respiratory treatments prescription than PD-directed protocol and it does not affect the outcomes of in-hospital pulmonary rehabilitation of COPD patients.