Gilbert Gottlieb

Experiential canalization of behavioral development: Results.

In exploring the possible experiential canalization of development, it was found that the mallard duck embryos contact call plays a canalizing role in species-specific perceptual development. When mallard ducklings were prevented from hearing the contact call, they were susceptible to developinga preference for an extraspecific maternal call over the mallard maternal call. Exposure to the contact call prevented the ducklings from developing a preference for the extraspecific maternal call. Thus, normally occurring experience, in concert with genetic and other activities, can canalize behavioral development. Canalizing influences account for developmental stability, so that what we think of as normal or typical for a species repeats itself generation after generation. In order for evolution to occur, through genetic mutation or otherwise, the canalizing influences associated with normal development must be overcome. Canalization is thus a conservative feature of development that prevents evolution from occurring in a ready fashion. My preced ing article (Gottlieb, 199 la)established the theoretical framework for examining the possibility that normally occurring experience can canalize behavioral development. The present article presents empirical evidence for the experiential canalization of species-specific maternal attachment. The present hypothesis is that normally occurring experience helps to achieve species-specific development by making the developing organism unresponsive to extraspecific influences. For example, if the mallard duck (Anas platyrhynchos) embryo is devocalized, the usually highly selective response to the mallard maternal call is weakened: After hatching, the duckling is as responsive to a chicken (Galfus gallus) maternal call as to a mallard maternal call in a simultaneous-choice test (Gottlieb, 1978). Exposing otherwise devocalized embryos to a recording of mallard embryo contact vocalizations causes them to show the usual preference for the mallard call versus the chicken call in the postnatal test (Gottlieb, 1985). Exposure to other types of sibling vocalizations in embryo, or exposure to the contact call after hatching, is ineffective, so the kind of experience and the timing of the experience are highly specific. If the experiential canalization hypothesis is correct, embryonic devocalization should make the mallard embryo and hatchling more susceptible to exposure to an extraspecific maternal call, assuming that the contact vocalization is acting as a canalizing or buffering experience. With the necessary control groups, five experimental conditions are necessary to test the canalization hypothesis, as indicated in Table 1. In Table 1, X indicates the predicted preference and X—-X indicates prediction of no preference. The two most critical

Social interaction with siblings is necessary for visual imprinting of species-specific maternal preferences in ducklings (Anas platyrhynchos).

This study was conducted to examine the influence of various social rearing experiences on the development of imprinted visual maternal preferences in domestic mallard ducklings (Anas platyrhynchos) during the first 3 days of postnatal life. Twenty-four-hour-old ducklings were allowed to follow a stuffed mallard hen for 30 min. This experience resulted in a visual preference for the familiar mallard hen over an unfamiliar stuffed redhead (Aythya americana) hen in simultaneous choice tests at 48 hr and 72 hr only if the ducklings were reared in conditions allowing unrestricted social interaction with siblings, as would normally occur in nature. No visual preference for the familiar mallard model was found at 48 hr or at 72 hr if ducklings were reared in social isolation but allowed to see another duckling, reared with one duckling, or reared in a group of ducklings but denied the opportunity for direct social interaction. These results demonstrate the importance of normal social experience in the development of the visual imprinting of filial behavior in ducklings. Imprinting studies have traditionally employed isolation rearing and ignored the precocial birds natural social context. Thus, the present findings raise doubts about the appropriateness of the usual methods of studying imprinting in the laboratory for an understanding of the process of filial imprinting in nature.

Neophenogenesis: A developmental theory of phenotypic evolution

An important task for evolutionary biology is to explain how phenotypes change over evolutionary time. Neo-Darwinian theory explains phenotypic change as the outcome of genetic change brought about by natural selection. In the neo-Darwinian account, genetic change is primary; phenotypic change is a secondary outcome that is often given no explicit consideration at all. In this article, we introduce the concept of neophenogenesis: a persistent, transgenerational change in phenotypes over evolutionary time. A theory of neophenogenesis must encompass all sources of such phenotypic change, not just genetic ones. Both genetic and extra-genetic contributions to neophenogenesis have their effect through the mechanisms of development, and developmental considerations, particularly a rejection of the commonly held distinction between inherited and acquired traits, occupy a central place in neophenogenetic theory. New phenotypes arise because of a change in the patterns of organism-environment interaction that produce development in members of a population. So long as these new patterns of developmental interaction persist, the new phenotype(s) will also persist. Although the developmental mechanisms that produce the novel phenotype may change, as in the process known as genetic assimilation, such changes are not necessary in order for neophenogenesis to occur, because neophenogenetic theory is a theory of phenotypic, not genetic, change.

Developmental intersensory interference: Premature visual experience suppresses auditory learning in ducklings☆

Abstract The present study was undertaken to test a recent hypothesis that in human and animal infants, premature stimulation in a later developing sensory system (e.g., vision) interferes with the normal functioning of an earlier developing system (e.g., audition) when the earlier system is still undergoing maturation. When mallard duck embryos are exposed to a mallard maternal assembly call they learn the features of the call as evidenced by their postnatal behavioral preference for it over an unfamiliar maternal call of the same species. However, if the embryos are given the opportunity to experience pattern vision prematurely, while undergoing auditory exposure to the call, they do not learn the maternal call. Further experiments showed that the interference only occurs when the exposure to the maternal call is concomitant with the premature visual experience. When otherwise prematurely visually stimulated duck embryos are exposed to the maternal call during periods of darkness they learn the call. Also, the premature visual experience does not interfere with the later postnatal auditory learning ability of such embryos. They are capable of learning the call when they are exposed to it after hatching. Consequently, the deleterious effect of premature visual experience would appear to be a transient phenomenon related to the distracting effects produced by concurrent auditory and visual stimulation that overtaxes the attentional abilities of the “preterm” duckling. Premature visual experience does not necessarily result in a persistent alteration in the developmental competence of the earlier developing auditory system, as predicted by a strong form of the developmental intersensory interference (DII) hypothesis. A weak form of the DII hypothesis is offered, which is predicated on transient, rather than permanent, effects involving momentary attentional difficulties caused by the concurrent stimulation of two immature or incompletely developed sensory systems.

Developmental intersensory interference: Augmented prenatal sensory experience interferes with auditory learning in duck embryos.

Embryos experiencing concurrent waterbed stimulation while being exposed to a mallard maternal call failed to learn the call, whereas embryos experiencing alternating waterbed and auditory stimulation did learn the call. However, when embryos were exposed to a lower level of concurrent waterbed stimulation-one that was closer to the normal level of proximal stimulation-they were able to learn the maternal call. Thus, an augmented level of proximal stimulation that departs less significantly from the normal range does not necessarily cause intersensory interference, even if it is higher than normal, suggesting a threshold that must be exceeded to cause interference

Influence of auditory experience on the development of brain stem auditory-evoked potentials in mallard duck embryos and hatchlings.

The development of brain stem auditory-evoked potentials (BAEP) was studied in devocalized ducklings reared in auditory isolation and in vocal ducklings exposed to enhanced species-specific auditory stimulation with embryonic contact-contentment calls (CTs). Thresholds and latency of BAEP wave P1 in the mute ducklings indicated that even short-term auditory deprivation affected the development of auditory sensitivity, substantially reducing the rate of decline in BAEP thresholds and latencies of P1, especially in the low-frequency (500 and 750 Hz) and high-frequency (above 2.0 kHz) ranges. The ducklings exposed to enhanced stimulation, on the other hand, showed an accelerated decline in BAEP thresholds and latencies of P1 across all test frequencies, with the most marked influence on low (below 1.5 kHz) and high (above 2.5 kHz) frequencies. The influence of species-specific auditory experience had its most potent effect during the embryonic critical period for postnatal auditory perceptual (behavioral) development, at which time the embryo produces and hears a special low-frequency (1.5-2.5 kHz) version of its own contact-contentment vocalization.

Development of species identification in ducklings: XII. Ineffectiveness of auditory self-stimulation in wood ducklings (Aix sponsa).

A previous study revealed that wood ducklings vocalize copiously when in auditory isolation. However, such self-stimulation appeared to be ineffective in maintaining their preference for the characteristically descending frequency-modulated (FM) notes of the wood duck maternal call. Only isolated birds that had been exposed to a recording of descending sib calls showed the normal preference for descending maternal notes in a choice test with descending and ascending maternal calls. In this study, the actual vocalizations of stimulated and unstimulated wood ducklings were examined in order to explore the possibility that there is a difference in the kind and/or amount of auditory self-stimulation in the two groups (e.g., the stimulated birds might produce more descending calls). Although the stimulated birds produced more ascending notes than the unstimulated birds, no differences were found in the overall vocal behavior, vocal reactivity, or specific kinds of frequency modulation produced by the birds that preferred the descending maternal call and the other birds that responded in the choice test. The absence of a difference in vocal production between the birds that preferred the descending call and the other responding birds supports the previous conclusion that self-stimulation apparently plays no role in the development or maintenance of the species-typical perceptual preference for the descending FM notes of the wood duck maternal call.

Social induction of malleability in ducklings

To test the hypothesis that social rearing may induce malleability, socially reared and socially isolated mallard duck, Anas platyrhynchos, embryos and hatchlings were exposed to the maternal call of a chicken, Gallus gallus domesticus, until 48h after hatching. The hatchlings were then tested with the chicken call versus the mallard maternal call at 48 and 65h. Social rearing before and after hatching led to the development of a persistent preference for the maternal call of the chicken. Social isolates did not develop a preference for the chicken call. The preference for the chicken call in the socially reared birds required both prenatal and postnatal exposure; socially reared birds exposed to the chicken call only before or only after hatching did not develop a preference for it. Social rearing overrode the usual canalizing influence of exposure to the embryos contact call. Socially reared birds spend most of their time asleep, so there may be a reduction in contact calling and/or less exposure to visual stimulation (less intersensory competition). Malleability is the requisite first step in the behavioural pathway to evolution.

Development of species identification in ducklings: XI. Embryonic critical period for species-typical perception in the hatchling

In the embryonic stages prior to hatching, the contact-contentment call of the Peking duck (domesticated Anas platyrhynchos) is more highly variable (2–6 notes/s) than it is after hatching (4–6 notes/s). The embryos must be exposed to the normally wide range of repetition rates of their contact-contentment call (2, 4, 6 notes/s) if their preference for the species maternal call is to be normal at 24 h after hatching. Exposure of muted embryos to the higher (4, 6 notes/s) or lower (2, 4 notes/s) portions of the normal range was ineffective. Thus the normally highly variable nature of the embryos vocalizations fits the requirements of its developing auditory system. An embryonic critical period was also demonstrated: when muted hatchlings were exposed to the rates typical of the postnatal period (4, 6 notes/s), or even the more widely variable rates of the embryonic period (2, 4, 6 notes/s), they failed to show a preference for the normal maternal call at 24 or 48 h after hatching. Thus the precise developmental linkage involves maturational stage as well as the representativeness of the stimulation.

Development of brainstem auditory pathway in mallard duck embryos and hatchlings.

SummaryThe development of the brainstem auditory evoked potential (BAEP) was studied in mallard duck (Anas platyrhynchos) embryos and hatchlings from 5–6 days before hatching through two days after hatching in response to tone pips of different frequencies. BAEPs showed a different time of onset and a different rate of development for low, middle, and high frequencies. Although auditory sensitivity in the mid-frequency range (1.0, 1.5, 2.0, and 3.0 kHz) appeared 1–2 days later than in the low-frequency range, development of the BAEPs in the mid-frequency range was almost complete by hatching. In contrast, the development of auditory sensitivity in the low- and high-frequency ranges continued to develop after hatching. Accelerated development of BAEPs to middle frequencies during the embryonic period and to high frequencies after hatching was correlated with the ducklings exposure to their own mid-frequency and high-frequency vocalizations before and after hatching, respectively.