Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating

Hermaphroditic individuals can produce both selfed and outcrossed progeny, termed mixed mating. General theory predicts that mixed-mating populations should evolve quickly toward high rates of selfing, driven by rapid purging of genetic load and loss of inbreeding depression (ID), but the substantial number of mixed-mating species observed in nature calls this prediction into question. Lower average ID reported for selfing than for outcrossing populations is consistent with purging and suggests that mixed-mating taxa in evolutionary transition will have intermediate ID. We compared the magnitude of ID from published estimates for highly selfing (r > 0.8), mixed-mating (0.2 ≤ r ≥ 0.8), and highly outcrossing (r < 0.2) plant populations across 58 species. We found that mixed-mating and outcrossing taxa have equally high average lifetime ID (δ= 0.58 and 0.54, respectively) and similar ID at each of four life-cycle stages. These results are not consistent with evolution toward selfing in most mixed-mating taxa. We suggest that prevention of purging by selective interference could explain stable mixed mating in many natural populations. We identify critical gaps in the empirical data on ID and outline key approaches to filling them.     

Social calls used by a leaf-roosting bat to signal location

Social calls in bats have many functions, including mate attraction and maintaining contact during flight. Research suggests that social calls may also be used to transfer information about roosts, but no studies have yet demonstrated that calls are used to actively attract conspecifics to roosting locations. We document the social calls used by Spix''s disc-winged bat (Thyroptera tricolor) to actively recruit group members to roosts. In acoustic trials, we recorded two sets of calls; one from flying individuals termed ‘inquiry calls’, and another from roosting bats termed ‘response calls’. Inquiry calls were emitted by flying bats immediately upon release, and quickly (i.e. 178 ms) elicited production of response calls from roosting individuals. Most flying bats entered the roost when roosting individuals responded, while few bats entered the roost in the absence of a response. We argue that information transfer concerning roost location may facilitate sociality in T. tricolor, given the ephemeral nature of roosting structures used by this species.     

A null mutation in TNIK defines a novel locus for intellectual disability

Intellectual disability (ID) is one of the most common disabilities and, although many genes have been implicated in its etiology, the genetic heterogeneity of ID continues to expand. The purpose of the study was to describe a novel autosomal recessive non-syndromic ID locus. Autozygome and linkage analysis, and exome sequencing followed by RNA and protein analysis of the candidate disease gene were performed. We describe two multiplex consanguineous families with non-syndromic ID phenotype, which maps to a critical linkage locus on 3q26. Exome sequencing of the index in each family revealed the same homozygous truncating mutation in TNIK that results in complete loss of the protein. TNIK is a kinase with a well-established role in dendrite development and synaptic transmission. The phenotype we observe in human patients who lack TNIK is consistent with the previously published Tnik ^?/? phenotype in the murine model. Our data strongly implicate TNIK deficiency in the causation of ID in humans.     

Does family language matter? The role of foreign language use and family social capital in the educational achievement of immigrant students in Germany

The role of ethnic resources in the educational success of immigrants is highly disputed. Combining arguments of segmented assimilation and Coleman's concept of family social capital, this study investigates whether speaking one's language of origin at home relates to achievement by facilitating the mobilization of resources or their transmission from parents to children. Mediating and moderating mechanisms are disentangled and empirically questioned in regression models that predict the mathematical competences of immigrant students from Turkey, Poland and the former Soviet Union. Based on data from the German National Educational Panel Study, the results contradict the assumption that foreign language use will contribute to education through mechanisms of social capital. Regardless of parental human capital or the group of origin, the language used at home does not affect the students’ learning when German language proficiency is accounted for.     

Turkish-language ability of children of immigrants in Germany: which contexts of exposure influence preschool children's acquisition of their heritage language?

A lot of research has been devoted to explaining immigrants' acquisition of the language of the receiving country. However, less attention has been paid to explaining the acquisition of the heritage language among children of immigrants. The most important determinant for young children is exposure to the language. Language exposure can occur in various contexts, such as within the family, during preschool, through peers or via media. Our empirical analysis therefore explores which of these contexts is most statistically significant for the acquisition of the heritage language among children of Turkish immigrants. Using data from the project Preschool Education and Educational Careers among Migrant Children, we show that all contexts are important at different age levels but the acquisition of the heritage language is mainly determined by the exposure to it within the family.     

Brevity is not always a virtue in primate communication

Semple et al. (Semple et al. in press, Biol. Lett. (doi:10.1098/rsbl.2009.1062)) argued that the ‘law of brevity’ (an inverse relationship between word length and frequency of use) applies not only to human language but also to vocal signalling in non-human primates, because coding efficiency is paramount in both situations. We analysed the frequency of use of signals of different duration in the vocal repertoires of two Neotropical primate species studied in the wild—the common marmoset (Callithrix jacchus) and the golden-backed uakari (Cacajao melanocephalus). The key prediction of the law of brevity was not supported in either species: although the most frequently emitted calls were relatively brief, they were not the shortest signals in the repertoire. The costs and benefits associated with signals of different duration must be appreciated to understand properly their frequency of use. Although relatively brief vocal signals may be favoured by natural selection in order to minimize energetic costs, the very briefest signals may be ambiguous, contain reduced information or be difficult to detect or locate, and may therefore be selected against. Analogies between human language and vocal communication in animals can be misleading as a basis for understanding frequency of use, because coding efficiency is not the only factor of importance in animal communication, and the costs and benefits associated with different signal durations will vary in a species-specific manner.     

The sound symbolism bootstrapping hypothesis for language acquisition and language evolution

Sound symbolism is a non-arbitrary relationship between speech sounds and meaning. We review evidence that, contrary to the traditional view in linguistics, sound symbolism is an important design feature of language, which affects online processing of language, and most importantly, language acquisition. We propose the sound symbolism bootstrapping hypothesis, claiming that (i) pre-verbal infants are sensitive to sound symbolism, due to a biologically endowed ability to map and integrate multi-modal input, (ii) sound symbolism helps infants gain referential insight for speech sounds, (iii) sound symbolism helps infants and toddlers associate speech sounds with their referents to establish a lexical representation and (iv) sound symbolism helps toddlers learn words by allowing them to focus on referents embedded in a complex scene, alleviating Quine''s problem. We further explore the possibility that sound symbolism is deeply related to language evolution, drawing the parallel between historical development of language across generations and ontogenetic development within individuals. Finally, we suggest that sound symbolism bootstrapping is a part of a more general phenomenon of bootstrapping by means of iconic representations, drawing on similarities and close behavioural links between sound symbolism and speech-accompanying iconic gesture.     

Campbell's Monkeys Use Affixation to Alter Call Meaning

Human language has evolved on a biological substrate with phylogenetic roots deep in the primate lineage. Here, we describe a functional analogy to a common morphological process in human speech, affixation, in the alarm calls of free-ranging adult Campbell''s monkeys (Cercopithecus campbelli campbelli). We found that male alarm calls are composed of an acoustically variable stem, which can be followed by an acoustically invariable suffix. Using long-term observations and predator simulation experiments, we show that suffixation in this species functions to broaden the calls'' meaning by transforming a highly specific eagle alarm to a general arboreal disturbance call or by transforming a highly specific leopard alarm call to a general alert call. We concluded that, when referring to specific external events, non-human primates can generate meaningful acoustic variation during call production that is functionally equivalent to suffixation in human language.     

Alarm calls elicit predator-specific physiological responses

Glucocorticoids regulate glucose concentrations and responses to unpredictable events, while also modulating cognition. Juvenile Belding''s ground squirrels (Urocitellus beldingi) learn to respond to whistle and trill alarm calls, warning of aerial and terrestrial predators, respectively, shortly after emerging from natal burrows at one month of age. Alarm calls can cause physiological reactions and arousal, and this arousal, coupled with watching adult responses, might help juveniles learn associations between calls and behavioural responses. I studied whether young show differential cortisol responses to alarm and non-alarm calls, using playbacks of U. beldingi whistles, trills, squeals (a conspecific control vocalization) and silent controls. Trills elicited very high cortisol responses, and, using an individual''s response to the silent control as baseline, only their response to a trill was significantly higher than baseline. This cortisol increase would provide glucose for extended vigilance and escape efforts, which is appropriate for evading terrestrial predators which hunt for long periods. Although whistles do not elicit a cortisol response, previous research has shown that they do result in bradycardia, which enhances attention and information processing. This is a novel demonstration of two physiological responses to two alarm calls, each appropriate to the threats represented by the calls.     

Effects of enhanced productivity of resources shared by predators in a food‐web module: Comparing results of a field experiment to predictions of mathematical models of intra‐guild predation

We compared the response to resource enhancement of a simple empirical model of intra‐guild predation (IGP) to the predictions of published, simple mathematical models of asymmetric IGP (a generalist IG Predator that feeds both on a specialist IG Prey and a Resource that it shares with the IG Prey). The empirical model was a food‐web module created by pooling species abundances across many families in a speciose community of soil micro‐arthropods into three categories: IG Predator (large predatory mites), IG Prey (small predatory mites), and a shared Resource (fungivorous mites and springtails). By pooling abundances of species belonging to broadly defined functional groups, we tested the hypothesis that IGP is a dominant organizing principle in this community. Simple mathematical models of asymmetric IGP predict that increased input of nutrients and energy to the shared Resource will increase the equilibrium density of Resource and IG Predator, but will decrease that of IG Prey. In a field experiment, we observed how the three categories of the empirical model responded to two rates of addition of artificial detritus, which enhanced the food of fungivores, the Resource of the IGP module. By the experiment''s end, fungivore densities had increased ~1.5× (ratio of pooled fungivore densities in the higher‐input treatment to plots with no addition of detritus), and densities of IG Predators had increased ~4×. Contrary to the prediction of mathematical models, IG Prey had not decreased, but instead had increased ~1.5×. We discuss possible reasons for the failure of the empirical model to agree with IGP theory. We then explore analogies between the behavior of the empirical model and another mathematical model of trophic interactions as one way to gain insights into the trophic connections in this community. We also propose one way forward for reporting comparisons of simple empirical and mathematical models.     

Mutations in USP9X Are Associated with X-Linked Intellectual Disability and Disrupt Neuronal Cell Migration and Growth

With a wealth of disease-associated DNA variants being recently reported, the challenges of providing their functional characterization are mounting. Previously, as part of a large systematic resequencing of the X chromosome in 208 unrelated families with nonsyndromic X-linked intellectual disability, we identified three unique variants (two missense and one protein truncating) in USP9X. To assess the functional significance of these variants, we took advantage of the Usp9x knockout mouse we generated. Loss of Usp9x causes reduction in both axonal growth and neuronal cell migration. Although overexpression of wild-type human USP9X rescued these defects, all three USP9X variants failed to rescue axonal growth, caused reduced USP9X protein localization in axonal growth cones, and (in 2/3 variants) failed to rescue neuronal cell migration. Interestingly, in one of these families, the proband was subsequently identified to have a microdeletion encompassing ARID1B, a known ID gene. Given our findings it is plausible that loss of function of both genes contributes to the individual''s phenotype. This case highlights the complexity of the interpretations of genetic findings from genome-wide investigations. We also performed proteomics analysis of neurons from both the wild-type and Usp9x knockout embryos and identified disruption of the cytoskeleton as the main underlying consequence of the loss of Usp9x. Detailed clinical assessment of all three families with USP9X variants identified hypotonia and behavioral and morphological defects as common features in addition to ID. Together our data support involvement of all three USP9X variants in ID in these families and provide likely cellular and molecular mechanisms involved.     

Acoustic Communication and Sound Degradation: How Do the Individual Signatures of Male and Female Zebra Finch Calls Transmit over Distance?

Background

Assessing the active space of the various types of information encoded by songbirds'' vocalizations is important to address questions related to species ecology (e.g. spacing of individuals), as well as social behavior (e.g. territorial and/or mating strategies). Up to now, most of the previous studies have investigated the degradation of species-specific related information (species identity), and there is a gap of knowledge of how finer-grained information (e.g. individual identity) can transmit through the environment. Here we studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation.

Methodology

We performed sound transmission experiments of zebra finches'' distance calls at various propagation distances. The propagated calls were analyzed using discriminant function analyses on a set of analytical parameters describing separately the spectral and temporal envelopes, as well as on a complete spectrographic representation of the signals.

Results/Conclusion

We found that individual signature is remarkably resistant to propagation as caller identity can be recovered even at distances greater than a hundred meters. Male calls show stronger discriminability at long distances than female calls, and this difference can be explained by the more pronounced frequency modulation found in their calls. In both sexes, individual information is carried redundantly using multiple acoustical features. Interestingly, features providing the highest discrimination at short distances are not the same ones that provide the highest discrimination at long distances.     

A comparative approach to the organization of vocal signals in noctural prosimians

Vocalizations and corresponding behavior patterns were recorded inGalago demidovii (Lorisidae), Microcebus murinus, andCheirogaleus medius (Cheirogaleidae). Physical characteristics of the calls were analyzed and calls correlated with their behavioral context. Based on these correlations an «advertisement» call can be identified in all three species. Interspecific comparison suggest that within the Prosimian suborder there are at least two different evolutionary pathways in the organization of this call and of the vocal repertoires in general. The Lorisid speciesG. demidovii conveys acoustic information mainly in pulsed calls, leading to an extreme amplitude-modulation. Individual characteristics are in temporal patterns of calls.C. medius andM. murinus, the Cheirogaleid species, use tonal calls and encode individual characteristics in frequency patterns. Despite the fundamental similarity in the call-structure of the two Cheirogaleid species different adaptations can be found to meet different ecological needs.     

THE ROLE OF INBREEDING DEPRESSION IN MAINTAINING THE MIXED MATING SYSTEM OF THE COMMON MORNING GLORY,IPOMOEA PURPUREA

Theoretical studies show that, although inbreeding depression (ID) will counterbalance the transmission advantage of selfing, it can only maintain a mixed mating system in plants when at least one of the following two conditions is met: (1) there is a positive association between selfing rates and the level of ID; and (2) ID is greater than 0.5 for the female component of fitness, while the average ID for male and female fitness is less than 0.5. This study tests whether these two conditions hold in the common morning glory, Ipomoea purpurea, which has a mixed mating system with 30% self-fertilization. Inbreeding depression was found in all but one fitness component measured in two groups of plants with distinct anther-stigma distances (ASD), a character that influences selfing rates. However, when examined separately, a negative association was found between selfing rates and ID; plants with large ASD (low-selfing-rate genotypes) tended to have higher ID than ones with small ASD (high-selfing-rate genotypes). Furthermore, the overall lifetime ID for male (12.5%) and female (24%) components of fitness, averaged across two ASD groups, were lower than what is necessary for ID to maintain an evolutionarily stable mixed mating system. Therefore, although inbreeding depression contributes to balancing the transmission advantage of selfing, it is not likely to be the primary mechanism maintaining the mixed mating system of I. purpurea. The contribution of other mechanisms is discussed.     

Asic3?/? Female Mice with Hearing Deficit Affects Social Development of Pups

Background

Infant crying is an important cue for mothers to respond adequately. Inappropriate response to infant crying can hinder social development in infants. In rodents, the pup-mother interaction largely depends on pup''s calls. Mouse pups emit high frequency to ultrasonic vocalization (2–90 kHz) to communicate with their dam for maternal care. However, little is known about how the maternal response to infant crying or pup calls affects social development over the long term.

Methodology/Principal Findings

Here we used mice lacking acid-sensing ion channel 3 (Asic3^−/−) to create a hearing deficit to probe the effect of caregiver hearing on maternal care and adolescent social development. Female Asic3^−/− mice showed elevated hearing thresholds for low to ultrasonic frequency (4–32 kHz) on auditory brain stem response, which thus hindered their response to their pups'' wriggling calls and ultrasonic vocalization, as well as their retrieval of pups. In adolescence, pups reared by Asic3^−/− mice showed a social deficit in juvenile social behaviors as compared with those reared by wild-type or heterozygous dams. The social-deficit phenotype in juvenile mice reared by Asic3^−/− mice was associated with the reduced serotonin transmission of the brain. However, Asic3^−/− pups cross-fostered to wild-type dams showed rescued social deficit.

Conclusions/Significance

Inadequate response to pups'' calls as a result of ASIC3-dependent hearing loss confers maternal deficits in caregivers and social development deficits in their young.     

Uncertainty and ignored information in the analysis of bat ultrasound: Bayesian approximation to the rescue

Bat ultrasound analysis has been around for several decades and it is one of the most important tools in studies of bat ecology. Discrimination between species is based on intra-specific features of echolocation calls. Identification of species and genera in audio files can be attempted either manually or through software which performs a fully automated discrimination between species. However, significant overlap in various features (e.g. frequencies of calls) exists between species and even genera. Species ID is therefore often not an absolute conclusion, but rather an opinion or best guess, as opposed to DNA tests or measurements on external characters of captured bats. To make things even worse, the probability of actually observing a bat of a given species in space and time is ignored when performing bat ultrasound analysis. This study introduces Bayesian approximation through a new method we have named Alternative Bayesian Bat Analysis (ABBA). We show, through a simple proof-of-concept example, the importance of adding information about the local composition of the bat community, hence making informed decisions regarding which species is most likely present in audio files. The superior performance of ABBA is also shown through an example using R code. Here, we use simulated data for three Pipistrellus spp., a genus with significant overlap in frequencies, but the code can easily be adapted to other bat species and genera worldwide. ABBA outperformed the non-Bayesian approach for all three species. The rare species in the simulated data set was super-inflated when using the non-Bayesian method. Further the results show, contrarily to common belief, that the frequency dominated by a given species in a data set, depends on the composition of the bat fauna and not just means and SDs reported in the literature. ABBA allows researchers to include all observations in statistical modeling, rather than excluding observations, an approach which can affect the reliability of studies. This study also, to a great extent, explains the poor performance of software attempting automated bat ID. Implementing Bayesian algorithms, and thereby allowing users to interact with the software, should significantly improve their performance.     

BIOACOUSTIC PUBLICATIONS, 1988

ABSTRACT

We examined vocalisations of a solitary subterranean rodent, the Silvery Mole-rat Heliophobius argenteocinereus (Bathyergidae). Seven true vocalisations and one mechanical vocalisation were identified. The main frequencies of the analysed sounds (0.34–13.17 kHz) match to a great extent the frequency range suitable for transmission in underground burrows. Due to the narrow frequency range of vocalisations, motivation is predominantly expressed by the rate of tonality rather than by frequency changes. The vocal repertoire of the Silvery Mole-rat perfectly matches to Morton's MS rules, i.e. that low-frequency and harsh vocalisations indicate hostility whereas high tonal calls signalise appeasement or fear. In comparison with social species, this solitary bathyergid produces fewer calls. It lacks contact and alarm calls, but has a rich repertoire of mating calls (mating ends with duet vocalization of male and female). Acoustic signals seem to play a major role in lowering natural aggressiveness during the mating period.     

Experimental evidence for group hunting via eavesdropping in echolocating bats

Group foraging has been suggested as an important factor for the evolution of sociality. However, visual cues are predominantly used to gain information about group members'' foraging success in diurnally foraging animals such as birds, where group foraging has been studied most intensively. By contrast, nocturnal animals, such as bats, would have to rely on other cues or signals to coordinate foraging. We investigated the role of echolocation calls as inadvertently produced cues for social foraging in the insectivorous bat Noctilio albiventris. Females of this species live in small groups, forage over water bodies for swarming insects and have an extremely short daily activity period. We predicted and confirmed that (i) free-ranging bats are attracted by playbacks of echolocation calls produced during prey capture, and that (ii) bats of the same social unit forage together to benefit from passive information transfer via the change in group members'' echolocation calls upon finding prey. Network analysis of high-resolution automated radio telemetry confirmed that group members flew within the predicted maximum hearing distance 94±6 per cent of the time. Thus, echolocation calls also serve as intraspecific communication cues. Sociality appears to allow for more effective group foraging strategies via eavesdropping on acoustical cues of group members in nocturnal mammals.     

Food-Associated Calling in Gorillas (Gorilla g. gorilla) in the Wild

Many nonhuman primates produce food-associated vocalizations upon encountering or ingesting particular food. Concerning the great apes, only food-associated vocalizations of chimpanzees (Pan troglodytes) and bonobos (Pan paniscus) have been studied in detail, providing evidence that these vocalizations can be produced flexibly in relation to a variety of factors, such as the quantity and quality of food and/or the type of audience. Only anecdotal evidence exists of eastern (Gorilla beringei) and western gorillas (Gorilla gorilla) producing food-associated vocalizations, termed singing or humming. To enable a better understanding of the context in which these calls are produced, we investigated and compared the vocal behavior of two free-ranging groups of western lowland gorillas (Gorilla g. gorilla) at Mondika, Republic of Congo. Our results show that (a) food-associated call production occurs only during feeding and not in other contexts; (b) calling is not uniformly distributed across age and sex classes; (c) calls are only produced during feeding on specific foods; and (d) normally just one individual gives calls during group feeding sessions, however, certain food types elicit simultaneous calling of two or more individuals. Our findings provide new insight into the vocal abilities of gorillas but also carry larger implications for questions concerning vocal variability among the great apes. Food-associated calls of nonhuman primates have been shown to be flexible in terms of when they are used and who they are directed at, making them interesting vocalizations from the viewpoint of language evolution. Food-associated vocalizations in great apes can offer new opportunities to investigate the phylogenetic development of vocal communication within the primate lineage and can possibly contribute novel insights into the origins of human language.     

Mutations in DDX3X Are a Common Cause of Unexplained Intellectual Disability with Gender-Specific Effects on Wnt Signaling

Intellectual disability (ID) affects approximately 1%–3% of humans with a gender bias toward males. Previous studies have identified mutations in more than 100 genes on the X chromosome in males with ID, but there is less evidence for de novo mutations on the X chromosome causing ID in females. In this study we present 35 unique deleterious de novo mutations in DDX3X identified by whole exome sequencing in 38 females with ID and various other features including hypotonia, movement disorders, behavior problems, corpus callosum hypoplasia, and epilepsy. Based on our findings, mutations in DDX3X are one of the more common causes of ID, accounting for 1%–3% of unexplained ID in females. Although no de novo DDX3X mutations were identified in males, we present three families with segregating missense mutations in DDX3X, suggestive of an X-linked recessive inheritance pattern. In these families, all males with the DDX3X variant had ID, whereas carrier females were unaffected. To explore the pathogenic mechanisms accounting for the differences in disease transmission and phenotype between affected females and affected males with DDX3X missense variants, we used canonical Wnt defects in zebrafish as a surrogate measure of DDX3X function in vivo. We demonstrate a consistent loss-of-function effect of all tested de novo mutations on the Wnt pathway, and we further show a differential effect by gender. The differential activity possibly reflects a dose-dependent effect of DDX3X expression in the context of functional mosaic females versus one-copy males, which reflects the complex biological nature of DDX3X mutations.