Maternal effects are ubiquitous generators of diverse phenotypic variation. Many maternal effects are based on hormonal signalling from mother to offspring and among other hormones steroids are critical signals. Since steroids play key roles in vertebrate reproduction and developmental differentiation their transmission from mother to embryo links generations, suggesting co-evolution of actions in mother and offspring. Birds have played a major role in generating knowledge about hormone-mediated maternal effects at the level of their functions and to a lesser extent their mechanisms. One of the classes of steroids that are transmitted from the ovary into the avian egg during yolk formation are androgens. The doses of androgens in eggs vary at multiple levels - within the eggs of a clutch, among clutches, among populations, and among species. Variation at these different levels has been addressed in relation to adaptive functions, such as parental favouritism, differential allocation, local adaptation, and life history strategies. However, only once we understand the integration of different maternal effect pathways and the mechanisms operating in mother and offspring will we fully understand the scope and limitations of maternal effects in evolutionary processes. I will review work on maternal effects conducted in my lab and in collaboration with others, refer to critical studies from other labs, and discuss basic developmental mechanisms of pleiotropic actions by which maternal steroids might influence offspring phenotype during the earliest embryo stages. [more]

Bird song is known as the acoustic analogue of the peacock’s tail, and is often used as a model in sexual selection studies. Most research has focused on between-individual differences in song traits and investigated questions about how aspects of male quality can be signalled and how these can be translated into fitness benefits. However, bird song is a very special in a sense that it can also show a considerable variation within individuals, while spatio-temporal patters define biologically important patterns of variations at the between-population level. My research group has been studying the song of the collared flycatcher (Ficedula albicollis), which has a modestly complex system with males using 15-50 different syllable types in their individual-specific repertoires that they vary with high plasticity. In our earlier studies, by adopting the classical focus from behavioural ecology on between-individual variations, we determined the information content of male repertoires its relationship with mating success. More recently, we investigate how songs change within individuals across different temporal windows (within- and between days, and between years) and how such reaction norms differ among individuals and what are the fitness consequences of this variation. At a higher level, we study compositional changes in song at the between-population level, which open horizons for understanding the dynamics of cultural evolution. In my talk, I will provide examples from our model species to demonstrate the evolutionary relevance of the complex hierarchical organization of bird song. [more]

Postnatal development includes progressive and regressive brain changes, some of them dependent on experience. Using a natural model of congenital deafness, the deaf white cat, our team has focused on effects of sensory experience on the structure and function of the auditory system. We use cochlear implant to test auditory function in deaf animals. Further, we provide deaf animals with a portable signal processor and a cochlear implant and induce hearing experience at different ages. We could demonstrate a delayed and altered cortical synaptic development in congenital deafness. Chronic electrical stimulation prevented many of the maturational deficits, provided stimulation was initiated within early sensitive periods. To investigate the reasons for sensitive periods, we studied visual function of the cortical auditory areas. We could demonstrate an areal-specific crossmodal reorganization in deafness. Although in the reorganized areas the auditory responsive neurons were not reduced in number, recruitment of even a limited number of neurons for visual tasks will reduce the computational capacity in the given area. Reduced feature sensitivity, as we have further shown, complicates the starting point for learning after restoration of hearing. Finally, corticocortical connections were studied both anatomically and functionally. Based on our layer-specific recordings in primary auditory cortex we previously suggested a corticocortical decoupling in deafness. Using tracer experiments and functional studies we find reduced bottom-up and top-down cortical information transfer in deafness. Such compromised top-down processing in the auditory cortex is likely participating on the closure of sensitive periods. [more]

The complex song of the common nightingale (Luscinia megarhynchos) can be considered a vocal peacock tail. In order to understand the evolution, function, and mechanisms of such elaborate courtship signals it is mandatory to study three domains: the signal inventory itself, traits that the signals are reliably indicating, and the biological relevance of this relation to receivers. We collected a longterm data set to study these domains in the song, mating decisions, and breeding biology of nightingales, following individuals across breeding seasons and years. We were able to relate specific song characteristics to individual traits such as age, body condition, or parental effort. We studied how Melatonin might potentially regulate nocturnal song activity and how song might serve as a prezygotic barrier in a hybridizing zone of twin species. Finally, I will provide examples on how the long-term documentation of life histories of individuals in their natural surroundings yielded in results of importance far beyond the study of communication and mating systems. [more]

Red is arguably the most conspicuous color in terrestrial habitats, and commonly involved in sexual, social or interspecific colour signalling. In birds, highly chromatic (“bright”) red integument (skin, scales, feathers) is typically caused by C4-ketocarotenoids (C4KC), such as astaxanthin, which are metabolically derived (‘ketolated’) from dietary yellow carotenoids, such as lutein or zeaxanthin. While this has been known for many decades, the molecular mechanism (the “C4-ketolase”) underlying this key innovation behind avian ornamentation and sexual dichromatism has remained obscure. Here we outline our recent discovery of a gene – CYP2J19 - that is responsible for red coloration in passerines, including multiple lineages of African ploceids and estrildids. High expression of CYP2J19 is found in the liver of male ploceids with red coloration in plumage or beak, and in the red beak of male estrildids. Intriguingly, CYP2J19 is also expressed in the retina, for pigmenting the red oil droplets, in all species studied so far, and this is likely its original function from which it has been recruited for red integumentary coloration in some lineages. Finally, CYP2J19 is a member of the large group of cytochrome P450 enzymes, which may indicate new mechanisms of honest signalling. Most important, however, along with our results on receiver biases for red in Euplectes, is the illustration of how striking diversification may derive from differential constraints rather than differential selection. [more]

The process by which we learn through observation of others has been associated with the acquisition of a range of complex skilled behaviors in humans as well as some animal species. Zebra finches, for instance, learn to produce their songs by listening to and trying to imitate a tutor, usually their father. What are the changes in the songbird brain that occur throughout development in order to shape the song learning process? It has been shown that a forebrain cortical region called HVC is centrally important for song learning and production. HVC contains premotor neurons that ultimately influence song-related musculature as well as a range of local circuit inhibitory interneurons. We recorded from premotor neurons in juvenile zebra finches while the birds were listening to their tutor’s song while carefully tracking the learning trajectory of those birds over several weeks. In inexperienced birds, we found that simply hearing the father’s song activates the same premotor neurons that the zebra finch will eventually use to produce his own song. Once the song had been mastered, however, premotor neurons stopped responding to the tutor song. In further experiments, we found that the responses to the tutor song were being actively suppressed by synaptic inhibition. To learn more about this inhibitory suppression, we directly measured the activity of inhibitory interneurons within HVC. The suppression of the tutor song through HVC inhibition was more strongly correlated with learning rather than developmental age. As the bird acquires his song and establishes his ideal motor program, this circuit became increasingly protected from any outside influences. This new insight not only completely redefines the role of inhibition in developing neural circuits, but also leads to the question about the origin of the auditory evoked inputs. [more]

The human infant is the most proficient vocal learner, and differs from his primate relatives in that he is specifically pre-adapted to acquire oral language. Melody (fundamental frequency contour) is a key entity to understand early language development. Infants from all cultures seem to pass through the same early stages of melody development at the same phase of their life history, long before vocabulary and grammar are established. Vocal development starts with an increasing complexification of melody over the first few months of life. The presentation will demonstrate what we mean by complexification of cry melody, how complex melodies are composed and modified, and why melody development marks crucial stages of early language acquisition. Along with adolescence, the neonatal period is a time when hormones may contribute to long-lasting, sexually dimorphic patterns of behavioural performance. This postnatal period of elevated hormone levels in both sexes is known as ‘mini-puberty”. The transitory surge of sex steroids within the first months of life is associated with dramatic developing brain changes, as well as the start of language-relevant vocal development in human infants. Recently, a significant positive association between mini-pubertal estradiol surges and early vocal performances (cry melody pattern, articulatory skills in babbling) has been demonstrated. This could bridge infant research to research in song birds, whose song learning has been postulated as modelling babbling in human infants [more]

Individual differences in cognition, emotion, and behaviour develop during ontogeny. Using a comparative approach, this contribution focuses on the modulation of behavioural profiles by the social environment in mammals. I review evidence that such shaping of behavioural profiles occurs from the prenatal phase through adolescence and beyond. Causation is discussed, in particular, how behavioural profiles are shaped by social stimuli through behavioural and neuroendocrine processes. Finally, function is addressed and it is argued that the shaping of behavioural profiles by social experience represents an effective mechanism for repeated and rapid adaptation during the life time. [more]

Humans are a remarkable species, especially because of the remarkable properties of their brain. Since the split from the chimpanzee lineage, the human brain has acquired abilities to better vocally learn and to use language. To better understand the molecular basis of these changes is of great biological and biomedical interest. However, all the about 16 million fixed genetic changes that occurred during human evolution are fully correlated with all molecular, cellular, anatomical and behavioral changes that occurred during this time. Hence, as humans and chimpanzees cannot be crossed or genetically manipulated, no direct evidence for linking particular genetic and molecular changes to human brain evolution can be obtained. Here, I sketch a framework how indirect evidence can be obtained and discuss in particular findings related to the speech-associated gene FOXP2. [more]

Studies using the chicken have made very significant contributions to understanding the development of vertebrates owing to the ease in manipulating the chicken embryo. The chick model system has become even more useful with the sequencing of the chicken genome and development of a robust method for transgenesis in the chicken (McGrew et al., 2004). It was also shown that migratory primordial germ cells from the chicken could be cultured in vitro for extended periods and used to generate transgenic chickens (van de Lavoir et al, 2006). My laboratory works on a type of stem cell in birds, the primordial germ cell, which is lineage restricted to producing spermatozoa and eggs of birds. These cells can be used to generate gene edited chickens, chicken which contain precise genetic changes in their genome. We have previously demonstrated that chicken primordial germ cells can be efficiently modified in vitro using transposable elements. I will discuss our use of new CRISPR/Cas9 vector to efficient edit single nucleotides in primordial germ cells and the use of sterile surrogate chicken hosts to increase germline transmission rates and decrease the time needed for production of genome edited chicken. A benefit of this research will be the technology to create bio-banks (frozen aviary) using germ cells. This is needed as the traditional methods used for species cryopreservation using semen and eggs are either inefficient or impossible in birds. Avian bio-banks will aid in the efforts to both manage and conserve both rare and industrial breeds of poultry. The future challenge is to extend biobanking to endangered bird species. [more]

Behavior, like beauty, is in the eyes of the beholder, and to understand how plants behave, one needs to appreciate their chemical prowess, as their behaviors are frequently played out on a chemical stage. Thanks to the long-term patient funding of the Max Planck Society, we have developed a fire-chasing native tobacco plant, Nicotiana attenuata, which grows in the Great Basin Desert, into an ecological model for the study of plant-ecological interactions in general and more specifically for the chemical behaviors that mediate this plant’s responses to biotic interactions that dominate the primordial agricultural niche. By training students in the lost art of natural history discovery, we have used the plant’s natural history interactions to phenotype transformed and recombinant inbred lines (RILs) of this plant, in a nature preserve in the plant’s native habitat, to understand the function of genes that mediate these chemical behaviors. This talk will describe what 5 native insect herbivores have taught us about behaviors that are essential for that plant function. The 5 insects come from different feeding guilds, attack different tissues at different developmental stages and have revealed different chemically-mediated behaviors that are essential for the plant’s survival. The over-arching take-home message of this talk is lifted from the playbook of the two founders of the discipline of Chemical Ecology (Thomas Eisner and Jerrold Meinwald), namely: the irreplaceable value of nature preserves as laboratories for the study of gene function. [more]

Estrildid finches (family: Estrildidae) are characterised by great intraspecific and intersexual variations in sexual traits, which include courtship song, dance and ornamental colourations of plumage. These features are expected to help us answer some questions about the evolution of sexual signals: (1) why multiple ornaments evolve in socially monogamous species; and (2) why, in certain species, males and females share identical sexual traits. In particular, I have been trying to understand the evolution of courtship dance, relying on phylogenetic comparative approaches along with intraspecific behavioural experiments. The results from a series of phylogenetic comparative studies show that courtship dance and the other sexual traits evolved almost independently. However, it is possible that dance display can function as an “amplifier” of plumage colour patterns, such as dots or stripes that are often possessed by Estrildid finches. These two visual signals (dance and colour patterns) are conspicuous in species with intraspecific brood parasitism, suggesting that reproductive cost/effort should be a factor that explains the evolution of elaborative visual sexual signals. Supporting this idea, both comparative and behavioural studies also show that nest material holding display evolved for parental cooperation of nest building. Males and females of Estrildids often exchange an identical courtship dance, which presumably plays a crucial role in mutual mate choice, pair-formation and pair-bonding. [more]

Constraining environments constitute a strong selective pressure potentially driving strategies to optimize the reliability of communication processes. In this perspective, the “Signal Structure Hypothesis” predicts that the structure of animal signals will differ depending on features of the habitat. For example and for vocal communications, the so-called “Acoustic Adaptation Hypothesis” predicts that bird songs optimized for long-range propagation in a forest should be slowly modulated in frequency and as low in frequency as the sender can produce. Since the susceptibility to propagation-induced modifications of emitted signals depends on their acoustic characteristics, the emitter also could enhance or on the contrary reduce its active space of communication by coding the information in more or less propagation-resistant parameters. I will show that this adjustment of the coding strategies according to the habitat can be experimentally demonstrated for the vocalizations of songbirds living in different habitats. Due to the variable spacing of territorial individuals, some information may be coded to degrade over short distance and some might be coded such that it transmits over long distance without much degradation. Thus, species-specific identity is encoded in propagation resistant acoustic features allowing individual to reach a wide audience and constitutes public information. Conversely, group identity, individual identity and motivation state are encoded by song features susceptible to propagation, a private information reserved for close neighbors or for the partner. [more]

Effective vocal communication between a sender and a recipient requires the fine tuning of a number of organ systems, including auditory organs as well as the motor circuitry that controls the vocal organs. These otherwise distinct organs are believed to occur as coevolved organ systems that must be matched between the senders and receivers to allow effective communication. Hummingbirds are highly vocal organisms that use vocal communication as major part of a larger multi-modal signaling strategy that also includes visual signals and feather-produced sounds. The bee hummingbirds are the most recent clade to have emerged in the hummingbird family, and include many of the smallest bodied hummingbirds that have radiated into north America. Bee hummingbirds are especially interesting in that vocal learning is present in some species but absent in others representing a significant loss of function of a trait that for many species is necessary for mate attraction and territory maintenance. We have been studying brain and syrinx anatomy of four bee hummingbirds that are abundant in Arizona. These include the Anna’s hummingbird which has a highly complex song, and its congener, the Costa’s hummingbird which has a less complex song. In addition, two species that are thought to have lost their song ability independently, the black-chinned hummingbird and the rufous hummingbird, are also included in our study. We use in situ hybridization for genes that are differential molecular markers of forebrain nuclei in songbird studies to understand these convergent brain circuits in hummingbirds. We note some interesting differences in vocal nuclei volume between the two singing species which may reflect the complexity of their vocal output, and the lack of a visible circuit in the non-singing hummingbirds. We also explore the use of other positive molecular markers of hummingbird neuroanatomy in an attempt to identify residual vocal forebrain structures in the non-singing species. Switching to bee hummingbird syrinx anatomy, we microCT scanned several excised vocal organs, followed by histological staining of thin tissue sections to provide a detailed look at the internal morphology of these smallest of avian sound sources. I will describe several traits that distinguish them from closely-related swifts and nightjars, and show a convergence with the syrinx of songbirds. These include an ossified and bifurcated tympanum, several accessory cartilages and multiple intrinsic muscle fascicles with different fiber orientations. Interestingly we note that singing species have larger syrinx structure with divergent morphology compared to the non-singing hummingbird species. Finally, I will discuss some future work to examine the auditory perception of hummingbird vocalizations, and finish by relating our work on the north American Bee lineage to a unique hummingbird species in se Brazil that vocalizes in a frequency range that all other avian species are believed not to hear. [more]

Songbirds need to form auditory memories not only of the tutor song for vocal imitation but also of many songs and calls of conspecifics for individual recognition. We know that songs and calls have idiosyncratic acoustical features and that birds can use these features to recognize specific individuals. In recent work, we have tested the memory capacity of zebra finches for caller ID based on songs and calls and found it to be impressively large: within one-week zebra finches are capable of recognizing ~16 individuals based on their song or distance call. The upper memory capacity of songbirds might actually be much higher, but it is difficult to assess in a laboratory experiment. Combining brain lesions and neurophysiological recordings, we have assessed the role of secondary auditory pallial areas NCM and CMM in memory formation and storage. We found that NCM plays an important role in these perceptual tasks. In future work, we plan on determining to what extend the auditory memories used for individual recognition in communication overlap with the auditory memories that songbirds use for vocal imitation. [more]

For any given species, the design of an animal’s visual system reflects the challenges of its ecological niche; thus, a promising approach to study visual system function is to probe the system with natural stimuli. Mice have become an important model in vision research, but it is still rarely considered that, compared to primates, they live in a different environment and therefore have different visual needs. For example, unlike primates, mice are dichromatic and perceive UV light. Moreover, the mouse retina is subdivided into a mostly “green” sensitive (peak at 510 nm) dorsal and UV sensitive (peak at 360 nm) ventral retina. Therefore, presenting naturalistic stimuli in laboratory settings to non-primate species, such as mice, is challenging.Under the assumption that a substantial fraction of mouse eye movements serves to stabilize the retinal image, we built a gimbal-stabilized, spectrally-calibrated hand-held camera to explore the natural habitat of mice in the relevant spectral bands. We intensity-calibrated the camera with LEDs of defined wavelengths and brightness using a power meter / spectrometer combination. The camera was moved close to the ground along mouse tracks and UV/green movies of the mouse habitat were recorded for different representative scenes and at different times of the day. By analysing contrast statistics of the movies, we found, for example, that contrast in the two chromatic channels (UV/ green) diverged greatly in the upper but not in the lower visual field. This resonates well with reports of a higher fraction of colour-opponent retinal ganglion cells in the ventral mouse retina and superior behavioural colour discrimination in the upper visual field. In addition, we found that during dusk and dawn, “predators” coming from the sky should be more easily detectable in the UV compared to the green channel, which emphasizes the UV’s role for mouse vision. Finally, we designed different unsupervised models, and when fitting them to our recordings, we mainly found color-opponent filters with training data of the upper visual field. In the last part of the talk, I will also show ongoing efforts to established a light-weight, head-mounted camera system, which can capture the visual environment from the perspective of freely roaming mice. [more]