Pathways in the emergence of developmental neuroethology: Antecedents to current views of neurobehavioral ontogeny

The historical forces that have contributed to our current views of neurobehavioral development (and thus to the fields of developmental psychobiology and neuroethology) are many and varied. Although similar statements might be made about almost any field of science, it is in particular true of this field, which represents a kind of mongrel discipline derived from at least three major sources (psychology, embryology, and neuroscience) and several more minor ones (including developmental psychology and psychiatry, psychoanalysis, education, zoology, ethology, and sociology). Although I attempt to demonstrate here how each of these sources may have influenced the emergence of a unified field of developmental psychobiology or developmental neuroethology, because the present article represents the first attempt of which I am aware to trace the history of these fields I am certain that there is considerable room for improvement, correction, and revision of the views expressed here. Accordingly, I consider this inaugural effort a kind of reconnaissance intended to trace a necessarily imperfect historic path for others to follow and improve upon. In the final analysis, I will be satisfied if this article only serves to underscore two related points: first is the value derived from historical studies of contemporary issues in development, and the second concerns the extent to which our current ideas and concepts about neurobehavioral development, ideas often considered new and contemporary, were already well known to those who came before us. The first point underscores the arguments expressed in the Introduction that the present must always be reconciled with the past, for the past is never entirely past. The second point returns full circle to an important thought expressed in the opening quotation to this article, namely, that even though our historic predecessors lacked much of the empirical facts available to us they were nonetheless able to attain a surprisingly deep understanding of neurobehavioral ontogeny. © 1992 John Wiley & Sons, Inc.     

Development of fluctuating asymmetry in tail feathers of the barn swallow Hirundo rustica

Fluctuating asymmetry represents usually small, random deviations from symmetry in bilateral morphological characters. The ontogeny of asymmetry in morphological characters may reveal information about developmental processes in a general sense. I studied the development of fluctuating asymmetry in feather characters of the barn swallow Hirundo rustica, that are developed repeatedly during the single annual moult, with the following results. First, the side developing a larger feather was found to be partially biased, as demonstrated by one side consistently developing a larger feather under natural and experimentally induced growth episode events. Second, asymmetric feathers were found to consist of asymmetric daily growth increments, and the size of the increments developing under different environmental conditions were positively correlated. Third, fluctuating asymmetries of feathers developing under different environmental conditions were positively correlated, although the level of asymmetry was larger under adverse environmental conditions. Fourth, individual asymmetries in tail length and growth bar length were unrelated to the duration of the developmental period, although late growth increments were smaller and more symmetric than early increments. These observations suggest that fluctuating asymmetry partially arises as a consequence of a random bias in the feather follicles and differences in environmental conditions during ontogeny of feathers.     

A simple model of the relationship between asymmetry and developmental stability

The relationship between developmental stability and morphological asymmetry is derived under the standard view that structures on each side of an individual develop independently and are normally distributed. I use developmental variance of sizes of parts, V_D, as the converse of developmental stability, and assume that V_D follows a gamma distribution. Repeatability of asymmetry, a measure of how informative asymmetry is about V_D, is quite insensitive to the variance in V_D, for example only reaching 20% when the coefficient of variation of V_D is 100%. The coefficient of variation of asymmetry, CV_FA, also increases very slowly with increasing population variation in V_D. CV_FA values from empirical data are sometimes over 100%, implying that developmental stability is sometimes more variable than any previously studied type of trait. This result suggests that alternatives to this model may be needed.     

The beak of the other finch: coevolution of genetic covariance structure and developmental modularity during adaptive evolution

The link between adaptation and evolutionary change remains the most central and least understood evolutionary problem. Rapid evolution and diversification of avian beaks is a textbook example of such a link, yet the mechanisms that enable beak''s precise adaptation and extensive adaptability are poorly understood. Often observed rapid evolutionary change in beaks is particularly puzzling in light of the neo-Darwinian model that necessitates coordinated changes in developmentally distinct precursors and correspondence between functional and genetic modularity, which should preclude evolutionary diversification. I show that during first 19 generations after colonization of a novel environment, house finches (Carpodacus mexicanus) express an array of distinct, but adaptively equivalent beak morphologies—a result of compensatory developmental interactions between beak length and width in accommodating microevolutionary change in beak depth. Directional selection was largely confined to the elimination of extremes formed by these developmental interactions, while long-term stabilizing selection along a single axis—beak depth—was mirrored in the structure of beak''s additive genetic covariance. These results emphasize three principal points. First, additive genetic covariance structure may represent a historical record of the most recurrent developmental and functional interactions. Second, adaptive equivalence of beak configurations shields genetic and developmental variation in individual components from depletion by natural selection. Third, compensatory developmental interactions among beak components can generate rapid reorganization of beak morphology under novel conditions and thus greatly facilitate both the evolution of precise adaptation and extensive diversification, thereby linking adaptation and adaptability in this classic example of Darwinian evolution.     

Linear and threshold-dependent expression of secondary sexual traits in the same individual: insights from a horned beetle (Coleoptera: Scarabaeidae)

Elaborate horns or horn‐like structures in male scarab beetles commonly scale with body size either (a) in a linear fashion with horn size increasing relatively faster than body size or (b) in a threshold‐dependent, sigmoid fashion; that is, males smaller than a certain critical body size develop no or only rudimentary horns, whereas males larger than the threshold size express fully developed horns. The development of linear vs. sigmoid scaling relationships is thought to require fundamentally different regulatory mechanisms. Here we show that such disparate regulatory mechanisms may co‐occur in the same individual. Large males of the south‐east Asian Onthophagus (Proagoderus) watanabei (Ochi & Kon) (Scarabaeidae, Onthophagini) develop a pair of long, curved head horns as well as a single thoracic horn. We show that unlike paired head horns in a large number of Onthophagus species, in O. watanabei the relationship between head horns and body size is best explained by a linear model. Large males develop disproportionately longer horns than small males, but the difference in relative horn sizes across the range of body sizes is small compared to other Onthophagus species. However, the scaling relationship between the thoracic horn and body size is best explained by a strongly sigmoid model. Only males above a certain body size threshold express a thoracic horn and males smaller than this threshold express no horn at all. We found a significant positive correlation between head and thoracic horn length residuals, contrary to what would be expected if a resource allocation tradeoff during larval development would influence the length of both horn types. Our results suggest that the scaling relationship between body size and horn length, and the developmental regulation underlying these scaling relationships, may be quite different for different horns, even though these horns may develop in the same individual. We discuss our results in the context of the developmental biology of secondary sexual traits in beetles. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 473–480.     

Architectural plasticity in a Mediterranean winter annual

Size variability in plants may be underlain by overlooked components of architectural plasticity. In annual plants, organ sizes are expected to depend on the availability and reliability of resources and developmental time. Given sufficient resources and developmental time, plants are expected to develop a greater number of large branches, which would maximize fitness in the long run. However, under restrictive growth conditions and environmental reliability, developing large branches might be risky and smaller branches are expected to foster higher final fitness. Growth and architecture of Trifolium purpureum (Papilionaceae) plants from both Mediterranean (MED) and semi-arid (SAR) origins were studied, when plants were subjected to variable water availability, photoperiod cues and germination timing. Although no clear architectural plasticity could be found in response to water availability, plants subjected to photoperiod cuing typical to late spring developed fewer basal branches. Furthermore, plants that germinated late were significantly smaller, with fewer basal branches, compared with plants which grew for the same time, starting at the beginning of the growing season. The results demonstrate an intricate interplay between size and architectural plasticities, whereby size modifications are readily induced by environmental factors related to prevalent resource availability but architectural plasticity is only elicited following the perception of reliable anticipatory cues.     

Effects of the egg incubation environment on turtle carapace development

Developing organisms are often exposed to fluctuating environments that destabilize tissue-scale processes and induce abnormal phenotypes. This might be common in species that lay eggs in the external environment and with little parental care, such as many reptiles. In turtles, morphological development has provided striking examples of abnormal phenotypic patterns, though the influence of the environment remains unclear. To this end, we compared fluctuating asymmetry, as a proxy for developmental instability, in turtle hatchlings incubated in controlled laboratory and unstable natural conditions. Wild and laboratory hatchlings featured similar proportions of supernumerary scales (scutes) on the dorsal shell (carapace). Such abnormal scutes likely elevated shape asymmetry, which was highest in natural nests. Moreover, we tested the hypothesis that hot and dry environments cause abnormal scute formation by subjecting eggs to a range of hydric and thermal laboratory incubation regimes. Shape asymmetry was similar in hatchlings incubated at five constant temperatures (26–30°C). A hot (30°C) and severely Dry substrate yielded smaller hatchlings but scutes were not overtly affected. Our study suggests that changing nest environments contribute to fluctuating asymmetry in egg-laying reptiles, while clarifying the conditions at which turtle shell development remains buffered from the external environment.     

榆黄毛萤叶甲的发育起点温度与有效积温的测定

【目的】有效防控榆黄毛萤叶甲Pyrrhalta maculicollis(Mots.)在吐鲁番地区的危害。【方法】本研究在室内设置22、25、28、31和34℃5个温度梯度,分别测定榆黄毛萤叶甲各虫态的发育历期,并以有效积温法则和"最小二乘法"计算出榆黄毛萤叶甲各虫态的发育起点温度和有效积温。【结果】卵、幼虫、蛹、产卵前期及全世代的发育起点温度分别为13.83、12.64、12.48、14.63和14.01℃,有效积温分别为83.99、186.32、121.50、185.42和550.54日·度。榆黄毛萤叶甲发育速率与温度的关系分别采用线性日度模型式和Logistic曲线模型式进行拟合,建立各虫态发育速率与温度关系模型。由Lagrange中值定理求出各虫态的发育最适温度、适宜温区,其全世代的分别为:Tmid为28.23℃、Tmin为14.36℃、Tmax为42.11℃。【结论】明确了榆黄毛萤叶甲各虫态的发育起点温度及有效积温,计算出了各虫态的理论发育最适温度及适宜温区,为准确预报榆黄毛萤叶甲发生期及有效防治提供理论依据。     

The axolotl mutants

The Mexican axolotl (Ambystoma mexicanum) has enjoyed wide use in experimental embryology for over 100 yr. Its usefulness has been extended into the area of developmental genetics largely due to the contributions of R. Briggs and R. R. Humphrey at Indiana University. To date over 30 mutants have been described, almost all of which affect development. Some of these have been discovered in inbred strains while others have been uncovered in recent Mexican imports. These mutants can be subdivided into several major classes. Maternal effect mutations lead to deficiencies in informational, structural, or metabolic components of the egg essential to early development prior to the time at which the embryo's own genome becomes active. In contrast, the developmental lethals affect later stages in embryogenesis when both morphogenetic and biochemical events are determined exclusively by the genotype of the embryo. Most lead to death at about feeding stage. Some, the cell lethals, are believed to suffer from fundamental metabolic defects affecting all parts of the embryo. Others affect the development of specific organs or tissues. The developmental nonlethals also affect specific systems, but ones that are not essential to survival. Some affect the development and survival of pigment cells and these, along with isozyme variants, are useful as markers in developmental experiments. A number of the mutants have been studied in detail, but others scarcely at all. The purpose of this review is to bring them to the attention of all developmental biologists in the hope that their potential will be even more widely recognized.     

红颈常室茧蜂蛹发育的形态特征

红颈常室茧蜂Peristenus spretus Chen et van Achterberg是一种绿盲蝽若虫的优势内寄生蜂,本研究利用超景深三维显微系统、显微镜观察了红颈常室茧蜂老熟幼虫发育特征、蛹形态特征及蛹发育后期卵巢的超微结构。结果表明:红颈常室茧蜂蛹期为12～15 d,其中雌蛹期比雄蛹期长2～3 d。根据其形态特征,可将蛹划分为预蛹期、第一蛹阶段、第二蛹阶段、第三蛹阶段。蛹期发育前9 d,蛹期组织结构开始分化形成,成蜂的外部形态基本显现,但性别难以区分;蛹期发育至10～14 d,可通过幼蜂体表颜色的变化或腹部末端的形状区分性别,在相同的适宜温度条件下,雌蜂比雄蜂颜色深,雌蜂腹部末端比较尖,有突出的产卵瓣,雄峰腹部末端钝圆,无凸起;雌蜂卵巢在化蛹后的第11天开始形成,卵巢初期的形状如细丝,此时卵巢管已开始初步分化,但卵室尚未分化;蛹发育至第12天时,卵巢管逐渐加粗,卵室开始分化;第13天时,卵巢管、卵室数量逐渐增多;第14天卵巢基部开始有少量成熟卵子产生,呈乳白色。10～12 d,雄蜂腹部末端绒毛逐渐增多,体壁变硬,逐渐角质化,虫体可活动,雄蜂胸部略带黑色,翅逐渐伸展开,整个虫体呈浅红棕色。本研究结果明确了红颈常室茧蜂蛹发育的形态变化过程,提出了蛹期雌雄区分的方法,叙述了蛹后期卵巢发育特征,为研究该蜂繁殖机理奠定了形态学基础。     

草地贪夜蛾的有效积温和发育始点及其发生世代预测

草地贪夜蛾Spodoptera frugiperda(J.E.Smith)自2019年6月入侵山东后,同年于山东部分地区发现其为害夏玉米,对当地玉米Zea mays L.的生产造成威胁.为了明确温度对该害虫的影响和在山东不同地区的发生世代数,进行了温度对其生长发育、生存的研究,测定了其适温范围、发育始点和有效积温,并按...     

Fluctuating Asymmetry as Risk Marker for Stress and Structural Defects in a Toxicologic Experiment

Fluctuating asymmetry (the directionally random asymmetry of bilateral structures, FA) is commonly used as a measure of developmental instability, and may increase with stress. As several studies reported a relation between FA and developmental abnormalities, we investigate whether FA could be an additional perhaps more sensitive marker of developmental toxicity. The aim of this work is analyzing patterns of FA in multiple traits in a large dataset of rabbit fetuses, which were prenatally exposed to a toxic compound and sacrificed just before natural delivery. Gravid females were exposed to three doses of this compound, inducing abnormalities in the fetuses at the high dose only. The average FA, however, was already higher than control in rabbit fetuses of the low‐dose group but did not further increase with higher concentrations. Moreover, the increase in FA differed between traits, with the hindlimbs showing the strongest response. In addition, we did not find any association between FA and the presence of fetal abnormalities at the individual level. Although these results suggest that FA may act as “an early warning system,” we did not find a dose–response relationship with increasing stress and effects were trait‐specific. Further testing is needed before FA may be considered as a sensitive marker in developmental toxicity studies.     

温度对马铃薯甲虫生长发育的影响

为了进一步明确温度对马铃薯甲虫Leptinotarsa decemlineata (Say)生长发育的影响, 在恒温条件, 研究了温度对马铃薯甲虫实验种群生长发育的影响。结果表明：温度对马铃薯甲虫各虫态的发育历期、存活率及种群的繁殖力有显著的影响。发育历期随温度的升高而缩短, 发育速率与温度呈显著的正相关。马铃薯甲虫世代存活率由大到小的顺序为27℃＞23℃＞19℃＞31℃＞15℃。27℃时成虫的产卵量最高, 单雌平均卵量为729.7粒;其次为23℃, 单雌平均卵量为639.2粒。并测得马铃薯甲虫卵、1龄幼虫、2龄幼虫、3龄幼虫、4龄幼虫、幼虫期、蛹期及全世代的发育起点温度分别为9.14, 10.50, 8.17, 10.28, 9.04, 9.59, 10.23和10.90℃, 有效积温分别为73.26, 43.22, 39.23, 34.05, 161.97, 273.02, 100.38和542.58日·度。据此认为温度对马铃薯甲虫实验种群的生长发育、存活和繁殖影响明显。     

Relationships among development, ecology, and morphology in the evolution of Echinoderm larvae and life cycles

The evolution of life cycles involves transitions between discrete states in one or more of the characters that comprise a developmental pattern. In this paper, we examine three of the major life cycle characters and the states for these characters. Using examples from echinoderms, we discuss the evolutionary transitions that have occurred in the type of morphogenesis, developmental habitat, and mode of nutrition during development. We evaluate the functional requirements associated with these transitions to infer the likelihood (frequency or rapidity) of change in a given character and of biases in the polarity of character state transitions. Using comparisons of closely related species, we evaluate the change between states in one character for dependence on the state of, or correlated changes in, other characters. Based on our analysis of congeneric species that differ in developmental habitat, we conclude that the transition between pelagic and benthic development is an ecological change that is independent of changes in morphogenesis and should be reversible. In contrast, the transition from feeding to nonfeeding development has been considered to be irreversible because it involves marked changes in larval morphology. We re-examine the transition between different modes of larval nutrition in light of recent studies that show that there exists a continuum of nutritional strategies between planktotrophy and lecithotrophy. This continuum is largely determined by variation in maternal investment and does not involve alterations in larval morphology. We suggest that the boundary between planktotrophy and lecithotrophy is frequently crossed and that this transition is reversible. Ecological changes represent the crossing of a functional threshold. Only after crossing the threshold, do larvae experience qualitatively different selective pressures that can lead to subsequent changes in morphology and development. Two different changes have occurred in the type of morphogenesis: the simplification of larval morphology that is associated with obligate (nonfeeding) lecithotrophy and the loss of the larval body plan in the evolution from indirect to direct development. It is the modification of morphology independent of the ecological changes that requires alterations in developmental processes, constrains evolutionary options, imposes irreversibility, and establishes the discrete nature of larval patterns in marine invertebrates.     

The chick optic tectum developmental stages. A dynamic table based on temporal‐ and spatial‐dependent histogenetic changes: A structural,morphometric and immunocytochemical analysis

Development is often described as temporal sequences of developmental stages (DSs). When tables of DS are defined exclusively in the time domain they cannot discriminate histogenetic differences between different positions along a spatial reference axis. We introduce a table of DSs for the developing chick optic tectum (OT) based on time‐ and space‐dependent changes in quantitative morphometric parameters, qualitative histogenetic features and immunocytochemical pattern of several developmentally active molecules (Notch1, Hes5, NeuroD1, β‐III‐Tubulin, synaptotagmin‐I and neurofilament‐M). Seven DSs and four transitional stages were defined from ED2 to ED12, when the basic OT cortical organization is established, along a spatial developmental gradient axis extending between a zone of maximal and a zone of minimal development. The table of DSs reveals that DSs do not only progress as a function of time but also display a spatially organized propagation along the developmental gradient axis. The complex and dynamic character of the OT development is documented by the fact that several DSs are simultaneously present at any ED or any embryonic stage. The table of DSs allows interpreting how developmental cell behaviors are temporally and spatially organized and explains how different DSs appear as a function of both time and space. The table of DSs provides a reference system to characterize the OT corticogenesis and to reliably compare observations made in different specimens. J. Morphol. 2011. © 2011 Wiley‐Liss, Inc.