Assessing the heritability of body condition in birds: a challenge exemplified by the great tit Parus major L. (Aves)

The definition and measurement of body condition are central to many ecological and evolutionary studies, yet the fundamental issue of whether variation in condition is inherited genetically remains unresolved. Furthermore, confusion has been caused through diverse uses of the word 'condition' itself. In this paper, we introduce the terms 'broad-sense condition' and 'narrow-sense condition' in an attempt to reduce this confusion. Because of the difficulty of measuring condition, field biologists use the mass relative to body size as a convenient index of condition. Such indices have also been used to estimate die heritability of condition. Using data from a wild great tit Parus major population, we demonstrate that a condition index may still contain residual variance that is due to body size. Hence, using a condition index to study the heritability of condition can give misleading results because that residual variance may itself be heritable. To avoid this problem, direct measures of condition, such as reserve tissues, should be used. We provide the first heritability estimates of direct measures of condition of full-grown birds in a wild population by the regression of mean offspring (both in winter, and when breeding) on mean parent (when breeding) values of two reserve tissues, fat and pectoral muscle, which are independent of body-size. A great tit's fat and muscle reserves in winter were significandy correlated with their respective values when the birds bred. However there was no evidence that the level of fat reserves in winter resembled those of the parents (when breeding), more than expected by chance. Slight resemblances between parents and offspring were detected for muscle in winter and for fat reserves when breeding. Muscle size in the breeding season provided stronger evidence for the inheritance of condition.     

Problem Concepts in Evolution Part I: Purpose and Design

In 1999, Scott suggested that evolution has existential repercussions for some students because they confuse methodological naturalism with philosophical naturalism: conflating the incapacity of scientific explanations to appeal to the supernatural with the idea that God must not exist. Unfortunately, part of the reason for the confusion involves terms that are used in a technical sense by evolutionary biologists but that also convey existential meanings to the general public. Such terms therefore should be used carefully by teachers, and their scientific meanings distinguished from their common meanings. We revisit these problem concepts, particularly in light of recent papers in cognitive psychology as they relate to understanding evolution, in a two-part series of articles. Here, in part I, we address design and purpose.     

The place of development in mathematical evolutionary theory

Development plays a critical role in structuring the joint offspring-parent phenotype distribution. It thus must be part of any truly general evolutionary theory. Historically, the offspring-parent distribution has often been treated in such a way as to bury the contribution of development, by distilling from it a single term, either heritability or additive genetic variance, and then working only with this term. I discuss two reasons why this approach is no longer satisfactory. First, the regression of expected offspring phenotype on parent phenotype can easily be nonlinear, and this nonlinearity can have a pronounced impact on the response to selection. Second, even when the offspring-parent regression is linear, it is nearly always a function of the environment, and the precise way that heritability covaries with the environment can have a substantial effect on adaptive evolution. Understanding these complexities of the offspring-parent distribution will require understanding of the developmental processes underlying the traits of interest. I briefly discuss how we can incorporate such complexity into formal evolutionary theory, and why it is likely to be important even for traits that are not traditionally the focus of evo-devo research. Finally, I briefly discuss a topic that is widely seen as being squarely in the domain of evo-devo: novelty. I argue that the same conceptual and mathematical framework that allows us to incorporate developmental complexity into simple models of trait evolution also yields insight into the evolution of novel traits.     

Some history of heredity-vs-environment, genetic inferiority at Harvard(?), and The (incredible) Bell Curve

This article discusses some historical and intellectual roots of American behaviorism in psychology and its anti-heredity, environmentalist bias, as well as the early ‘justification’ for pure line theory in genetics and some interrelations between the two fields. Next, I discuss the heritability concept, its promotion, its critique and the importance of distinguishing it from, rather than confusing or conflating it with, the heredity concept. Then, briefly I consider some of the history and problems associated with the intelligence concept, as well as the capital importance of biological controls in studies of human heredity. And finally, I document the incredibility of The Bell Curve and the appalling inadequacy of its reception. This revised version was published online in August 2006 with corrections to the Cover Date.     

On models and muddles of heritability

One reason for the astonishing persistence of the IQ myth in the face of overwhelming prior and posterior odds against it may be the unbroken chain of excessive heritability claims for ‘intelligence’, which IQ tests are supposed to ‘measure’. However, if, as some critics insist, ‘intelligence’ is undefined, and Spearman's g is beset with numerous problems, not the least of which is universal rejection of Spearman's model by the data, then how can the heritability of ‘intelligence’ exceed that of milk production of cows and egg production of hens? The thesis of the present review paper is that the answer to this riddle has two parts: (a) the technical basis of heritability claims for human behavior is just as shaky as that of Spearman's g. For example, a once widely used ‘heritability estimate’ turns out to be mathematically invalid, while another such estimate, though mathematically valid, never fits any data; and (b) valid technical criticisms of flawed heritability claims typically are met with stubborn editorial resistance in the main stream journals, which tends to calcify such misinformation.     

Symplastic growth and symplasmic transport

In current usage, the adjective symplastic has two different meanings: in the term, symplastic growth, as defined by Priestley; and in discussions of transport through the symplast, as defined by Münch. To avoid confusion, it is recommended that symplastic be reserved to characterize growth deformation, that symplasmic be used to refer to transport through the symplasm, and apoplasmic, to refer to the apoplasm.     

From survivors to replicators: evolution by natural selection revisited

For evolution by natural selection to occur it is classically admitted that the three ingredients of variation, difference in fitness and heredity are necessary and sufficient. In this paper, I show using simple individual-based models, that evolution by natural selection can occur in populations of entities in which neither heredity nor reproduction are present. Furthermore, I demonstrate by complexifying these models that both reproduction and heredity are predictable Darwinian products (i.e. complex adaptations) of populations initially lacking these two properties but in which new variation is introduced via mutations. Later on, I show that replicators are not necessary for evolution by natural selection, but rather the ultimate product of such processes of adaptation. Finally, I assess the value of these models in three relevant domains for Darwinian evolution.     

The behaviors of some heritability estimators in the complete absence of genetic factors.

Heritability is an important concept in quantitative genetics and is widely used in human genetics. A high or even a moderate value of heritability estimate is usually taken as evidence for a genetic component for a quantitative trait. In this paper, the behaviors of some correlation-based heritability estimators are reexamined under the assumption of complete absence of any genetic factors. It turns out that when monozygotic (MZ) twins (or full sibs) are environmentally more similar than dizygotic twins (or half sibs), or when there is placement bias in MZ twins reared apart, those correlation-based heritability estimates can lead to nonnegligible or even high heritability values, even when genetic factors are completely absent. These alarming results suggest that extreme care should be exercised when using these heritability estimators.     

Is optimism optimal? Functional causes of apparent behavioural biases

We review the use of the terms ‘optimism’ and ‘pessimism’ to characterize particular types of behaviour in non-human animals. Animals can certainly behave as though they are optimistic or pessimistic with respect to specific motivations, as documented by an extensive range of examples in the literature. However, in surveying such examples we find that these terms are often poorly defined and are liable to lead to confusion. Furthermore, when considering behaviour within the framework of optimal decision theory using appropriate currencies, it is often misleading to describe animals as optimistic or pessimistic. There are two common misunderstandings. First, some apparent cases of biased behaviour result from misidentifying the currencies and pay-offs the animals should be maximising. Second, actions that do not maximise short-term pay-offs have sometimes been described as optimistic or pessimistic when in fact they are optimal in the long term; we show how such situations can be understood from the perspective of bandit models. Rather than describing suboptimal, unrealistic behaviour, the terms optimism and pessimism are better restricted to informal usage. Our review highlights the importance of choosing the relevant currency when attempting to predict the action of natural selection.     

When is a cladist not a cladist?

The term “cladist” has distinct meanings in distinct contexts. Communication between philosophers, historians, and biologists has been hindered by different understandings of the term in various contexts. In this paper I trace historical and conceptual connections between several broadly distinct senses of the term “cladist”. I propose seven specific definitions that capture distinct contemporary uses. This serves to disambiguate some cases where the meaning is unclear, and will help resolve apparent disagreements that in fact result from conflicting understandings of the term.     

Warning signals evolve to disengage Batesian mimics

Prey that are unprofitable to attack are typically conspicuous in appearance. Conventional theory assumes that these warning signals have evolved in response to predator receiver biases. However, such biases might be a symptom rather than a cause of warning signals. We therefore examine an alternative theory: that conspicuousness evolves in unprofitable prey to avoid confusion with profitable prey. One might wonder why unprofitable prey do not find a cryptic means to be distinct from profitable prey, reducing both their risk of confusion with profitable prey and their rate of detection by predators. Here we present the first coevolutionary model to allow for Batesian mimicry and signals with different levels of detectability. We find that unprofitable prey do indeed evolve ways of distinguishing themselves using cryptic signals, particularly when appearance traits can evolve in multiple dimensions. However, conspicuous warning signals readily evolve in unprofitable prey when there are more ways to look different from the background than to match it. Moreover, the more unprofitable the prey species, the higher its evolved conspicuousness. Our results provide strong support for the argument that unprofitable species evolve conspicuous signals to avoid confusion with profitable prey and indicate that peak shift in conspicuousness-linked traits is a major factor in its establishment.     

Different terms used to describe "red tides"

An event characterized by sudden increase in phytoplankton population, in the sea or aqueous environment, is often designated by different Spanish terms that attempt to describe the nature, aspect, characteristics, and/or properties of such phenomena. In this communication, we discuss the convenience of reaching an agreement among the Spanish-speaking scientific community to use a simple Spanish term that could be much more informative and accurate when referring to Harmful Algal Blooms (HABs), in general. Summarizing the different Spanish terms historically employed to describe the proliferation of noxious phytoplankton in the sea, we propose "Proliferación Microalgal Nociva" (PMN = HAB) as a term that, on the basis of its etymological meaning could be considered correct. Its use could help to avoid the prevailing confusion in our language caused by different misleading terms now employed when referring to a Harmful Algal Bloom event.     

The Natural Experiment

Many of you, reading the title of this report, probably felt a certain confusion about this new, unusual term natural experiment. To dispel this quite natural confusion, let me say immediately that I am proposing this term to designate special investigatory techniques situated somewhere between external, objective observation, on the one hand, and a man-devised laboratory experiment (at present referred to as a psychological experiment), on the other. These original techniques, different from both the first and the second, are actually not completely new and unusual but, on the contrary, are well known to every one of you in their rudimentary form. Considered in more detail, they might perhaps be of considerable interest both theoretically and practically. It is for this reason that I decided to propose a new term to designate them. One cannot, of course, in such a brief report attempt to outline all the possible applications of this method to all the phenomena to which it could be applied; hence, I shall focus on an area that is more familiar to me and, moreover, seems to be especially suited for conducting a natural experiment, namely, research on personality or individuality.     

Pleuston and neuston: On the categories of organisms in the uppermost pelagial

The development of the connotations attached to the terms pleuston, neuston, and some of their derivatives is outlined. In the marine literature, the term hyponeuston has presently two principal. quite different meanings: organisms attached from below to the surface film and largely supported by it, and organisms frequenting the upper decimeter of the sea. To reduce the ensuing confusion in the marine realm and to maintain uniformity of aquatic terminology, the term endopleuston is proposed as a replacement for the second, recently acquired meaning of hyponeuston. Another new term, exopleuston, refers to positively buoyant organisms with dry upper surfaces which, however, live principally underwater, in the habitat of the endopleuston. The pleustal is recognized as the habitat of these organisms. It may be useful to regard it as a category. of equal rank the epipelagial or bathypelagial.     

Rethinking heredity, again

The refutation of 'soft' inheritance and establishment of Mendelian genetics as the exclusive model of heredity is widely portrayed as an iconic success story of scientific progress. Yet, we are witnessing a re-emergence of debate on the role of soft inheritance in heredity and evolution. I argue that this reversal reflects not only the weight of new evidence but also an important conceptual change. I show that the concept of soft inheritance rejected by 20th-century genetics differs fundamentally from the current concept of 'nongenetic inheritance'. Moreover, whereas it has long been assumed that heredity is mediated by a single, universal mechanism, a pluralistic model of heredity is now emerging, based on a recognition of multiple, parallel mechanisms of inheritance.     

Pattern, process and the evolution of meaning: species and units of selection

Many of the fundamental concepts of biology lack consensual, precise definitions. Partly, this is due to a contrast between our discrete language and the continuous character of nature. Some debates over these concepts are confounded by the use of the same terms with different specific meanings, indicating a possible need for an expanded scientific lexicon. Words have their own histories, and frequently scientific terms with a vernacular origin retain associated vestigial meanings. Even terms newly coined within science have histories and changing meanings, which can lead to confusion among debaters. Debates over concepts are further confounded when the same terms are used in different fields of biology, with distinct (even conflicting) objectives, and by biologists with different approaches and perspectives. I illustrate these issues by considering the debate over the concept of species and the unit of selection.     

Problems of terminology in the teaching of plant water relations

The considerable variation and confusion in terminology used in the teaching of plant water relations is discussed. The concept of water potential is described briefly and compared with the older concepts of diffusion pressure deficit and suction pressure. The advantages of using water potential terminology are considered. Reference is made to some well-known student texts to illustrate the conflicting meanings of osmotic terms and symbols, and attention is drawn to the problems which arise when authors mix old and new terms. It is recommended that the new terminology should be incorporated into school examination syllabuses and textbooks as soon as possible.     

Population and quantitative genetics of regulatory networks

I evolved boolean regulatory networks in a computer simulation. I varied mutation, recombination, the size of the network, and the number of connections per node. I measured the performance of networks and the heritability and epistasis of genetic effects. Networks of intermediate connectivity performed best. The distinction between metabolic and quantitative genetic additivity explained some of the variation in performance. Metabolic additivity describes the interaction between changes in a single network, whereas quantitative genetic additivity measures the consistency of phenotypic effect caused by gene substitution in randomly chosen members of the population. I analysed metabolic additivity by the distribution of epistatic effects of pairs of mutations in individual networks. I measured quantitative genetic additivity by heritability. Highly connected networks had greater metabolic additivity for perturbations to individual networks, but had lower additivity when measured by the average effect of a gene substitution (heritability). The lower heritability of highly connected nets appeared to reduce the effectiveness of recombination in searching evolutionary space.