Causal mechanisms of evolution and the capacity for niche construction

Ernst Mayr proposed a distinction between “proximate”, mechanistic, and “ultimate”, evolutionary, causes of biological phenomena. This dichotomy has influenced the thinking of many biologists, but it is increasingly perceived as impeding modern studies of evolutionary processes, including study of “niche construction” in which organisms alter their environments in ways supportive of their evolutionary success. Some still find value for this dichotomy in its separation of answers to “how?” versus “why?”questions about evolution. But “why is A?” questions about evolution necessarily take the form “how does A occur?”, so this separation is illusory. Moreover, the dichotomy distorts our view of evolutionary causality, in that, contra Mayr, the action of natural selection, driven by genotype-phenotype-environment interactions which constitute adaptations, is no less “proximate” than the biological mechanisms which are altered by naturally selected genetic variants. Mayr’s dichotomy thus needs replacement by more realistic, mechanistic views of evolution. From a mechanistic viewpoint, there is a continuum of adaptations from those evolving as responses to unchanging environmental pressures to those evolving as the capacity for niche construction, and intermediate stages of this can be identified. Some biologists postulate an association of “phenotypic plasticity” (phenotype-environment covariation with genotype held constant) with capacity for niche construction. Both “plasticity” and niche construction comprise wide ranges of adaptive mechanisms, often fully heritable and resulting from case-specific evolution. Association of “plasticity” with niche construction is most likely to arise in systems wherein capacity for complex learning and behavioral flexibility have already evolved.     

The Creativity of Natural Selection? Part I: Darwin,Darwinism, and the Mutationists

This is the first of a two-part essay on the history of debates concerning the creativity of natural selection, from Darwin through the evolutionary synthesis and up to the present. Here I focus on the mid-late nineteenth century to the early twentieth, with special emphasis on early Darwinism and its critics, the self-styled “mutationists.” The second part focuses on the evolutionary synthesis and some of its critics, especially the “neutralists” and “neo-mutationists.” Like Stephen Gould, I consider the creativity of natural selection to be a key component of what has traditionally counted as “Darwinism.” I argue that the creativity of natural selection is best understood in terms of (1) selection initiating evolutionary change, and (2) selection being responsible for the presence of the variation it acts upon, for example by directing the course of variation. I consider the respects in which both of these claims sound non-Darwinian, even though they have long been understood by supporters and critics alike to be virtually constitutive of Darwinism.     

Evolution of increased competitiveness in cows trades off with reduced milk yield,fertility and more masculine morphology

In some species females compete for food, foraging territories, mating, and nesting sites. Competing females can exhibit morphological, physiological, and behavioral adaptations typical of males, which are commonly considered as secondary sexual traits. Competition and the development of traits increasing competitiveness require much energy and may exert adverse effects on fecundity and survival. From an evolutionary perspective, positive selection for increased competitiveness would then result in evolution of reduced values for traits related to fitness such as fecundity and survival. There is recent evidence for such evolutionary trade‐offs involving male competition, but no study has considered competing females so far. Using data from competitions for dominance in cows (Bos taurus), we found negative genetic correlations between traits providing success in competition, that is, fighting ability and fitness traits related to milk production and with fertility (the inverse of parity‐conception interval). Fighting ability also showed low but positive genetic correlations with “masculine” morphological traits, and negative correlations with “feminine” traits. A genetic change in traits over time has occurred due to selection on competitiveness, corresponding to an evolutionary process of “masculinization” counteracting the official selection for milk yield. Similar evolutionary trade‐off between success in competition and fitness components may be present in various species experiencing female competition.     

Formal Darwinism

Two questions are raised for Grafen’s formal darwinism project of aligning evolutionary dynamics under natural selection with the optimization of phenotypes for individuals of a population. The first question concerns mean fitness maximization during frequency-dependent selection; in such selection regimes, not only is mean fitness typically not maximized but it is implausible that any parameter closely related to fitness is being maximized. The second question concerns whether natural selection on inclusive fitness differences can be regarded as individual selection or whether it leads to a departure from the central motivation that led to the formal darwinism project, viz., to show that “Darwinian” evolution through individual selection leads to “good design” or phenotypic adaptation through trait optimization.     

The individuality of the species: A Darwinian theory? — from Buffon to Ghiselin, and back to Darwin

Since the 1970s, there has been a tremendous amount of literature on Ghiselin's proposal that “species are individuals”. After recalling the origins and stakes of this thesis in contemporary evolutionary theory, I show that it can also be found in the writings of the French naturalist Buffon in the 18th Century. Although Buffon did not have the conception that one species could be derived from another, there is an interesting similarity between the modern argument and that of Buffon regarding the “individuality of species’. The analogy is strong enough to force us to recognize that genuine evolutionary (or Darwinian) questions might be of secondary importance in the discussion. In consequence, the third section of the paper proposes an alternative schema for the “logical structure” of the Darwinian concept of species. Darwin distinguished the problem of the designation of a concrete species, and the problem of its signification of species within his theory of descent? The resulting notion of species involves a logical structure based on the fusion of the logical operations of classification and ordering. The difficulty — and interest — is that this interpretation of species does not entail any precise operational definition of species; it can only tell us what the ultimate signification of classification is within the theory of descent with modification through natural selection.     

Can an Environmental Indicator valid both at the local and global scales be derived on a thermodynamic basis?

Environmental considerations are becoming an essential part of any energy conversion assessment: the concept of “environmental impact” has substantially evolved in the last decade, from a pure “assessment of ecological damage” (pollution) to a more complex and omnicomprehensive, but at the same time more detailed, examination of the local and global implications of the interactions of anthropic processes with the biosphere at large. This paper proposes an Environmental Indicator derived strictly on thermodynamic concepts and defines a procedure for its application to both local and global scales in a rationally sound and convenient fashion. The new indicator is the extended exergy cost, ee_C, and is a measure of the primary (exergy) resources embodied in a material or immaterial product. It is shown that such an EI can successfully include the “externalities” (Labor, Capital and Environmental Remediation costs) that affect the planning of anthropic energy conversion systems, and that it can also be employed to assess the evolutionary patterns of natural systems. Some conceptual examples of application are provided to demonstrate that ee_C is indeed a useful tool for the quantification of real -i.e., resource based- environmental costs and for their proper internalization in both engineering and system studies.     

NONADAPTIVE PROCESSES CAN CREATE THE APPEARANCE OF FACULTATIVE CHEATING IN MICROBES

Adaptations to social life may take the form of facultative cheating, in which organisms cooperate with genetically similar individuals but exploit others. Consistent with this possibility, many strains of social microbes like Myxococcus bacteria and Dictyostelium amoebae have equal fitness in single‐genotype social groups but outcompete other strains in mixed‐genotype groups. Here we show that these observations are also consistent with an alternative, nonadaptive scenario: kin selection‐mutation balance under local competition. Using simple mathematical models, we show that deleterious mutations that reduce competitiveness within social groups (growth rate, e.g.) without affecting group productivity can create fitness effects that are only expressed in the presence of other strains. In Myxococcus, mutations that delay sporulation may strongly reduce developmental competitiveness. Deleterious mutations are expected to accumulate when high levels of kin selection relatedness relax selection within groups. Interestingly, local resource competition can create nonzero “cost” and “benefit” terms in Hamilton's rule even in the absence of any cooperative trait. Our results show how deleterious mutations can play a significant role even in organisms with large populations and highlight the need to test evolutionary causes of social competition among microbes.     

Mort ou persistance du darwinisme ? Regard d’un épistémologue

The article examines why evolutionary biologists have been haunted by the question whether they are “Darwinian” or “non-Darwinian” ever since Darwin's Origin of species. Modern criticisms addressed to Darwinism are classified into two categories: those concerning Darwin's hypothesis of “descent with modification” and those addressed to the hypothesis of natural selection. In both cases, although the particular models that Darwin proposed for these two hypotheses have been significantly revised and expanded, Darwin's general framework has constrained and canalized evolutionary research, in the sense that it has settled an array of possible theoretical choices. Gould's changing attitudes regarding Darwinism is taken as a striking illustration of this interpretation.     

Towards a genetic theory for the evolution of the sex ratio. III. Parental and sibling control of brood investment ratio under partial sib-mating

Models of sex ratio evolution under partial sib-mating are investigated in haplodiploids and diploids. In the cases of parental and sibling control of the brood investment ratio between the sexes in diploids, we find that the “unbeatable” investment ratio obtained by W. D. Hamilton (Science156, 477–488) for his local mate competition model corresponds in our inbreeding models to a weak form ESS (evolutionary stable strategy) fixation state and also to the population investment ratio at certain internal equilibria of our models. For haplodiploids, “strong form ESS” values exist under inbreeding in models involving father and sister control. Under brother and mother control, however, the ESS derived from local mate competition models is unstable in our inbreeding models to the introduction of any other investment ratio. We stress important qualitative differences between models involving local mate competition and inbreeding.     

Evolutionary causes of male-biased sexual size dimorphism from a female perspective in the seed bug Togo hemipterus (Heteroptera: Lygaeidae)

Sexual size dimorphisms (SSDs) in body size are expected to evolve when selection on female and male sizes favors different optima. Many insects show female-biased SSD that is usually explained by the strong fecundity advantage of larger females. However, in some insects, males are as large as or even larger than females. The seed bug Togo hemipterus (Scott) also exhibits a male-biased SSD in body size. Many studies that have clarified the evolutionary causes of male-biased SSD have focused only on male advantages due to male–male competition. To clarify the evolutionary causes of male-biased SSD in body size, we should examine the degree of not only the sexual selection that favors larger males but also natural selection that is acting on female fecundity. The obtained results, which showed higher mating acceptance rates to larger males, implies that females prefer larger males. No significant relationship was detected between female body size and fecundity; body size effects on female fecundity were weak or undetectable. We conclude that male-biased SSD in T. hemipterus can be accounted for by a combination of sexual selection through male–male competition and female choice favoring large males, plus weak or undetectable natural selection that favors large females due to a fecundity advantage.     

THE GENETICS OF ADAPTATION: THE GENETIC BASIS OF RESISTANCE TO WASP PARASITISM IN DROSOPHILA MELANOGASTER

There have been very few genetic analyses of “natural” adaptations, that is, those not involving artificial selection or responses to human disturbance. Here we analyze the genetic basis of geographic variation in Drosophila melanogaster's resistance to parasitism by a wasp, Asobara tabida. Our results suggest that population differences in ability to encapsulate parasitoid eggs have a fairly simple genetic basis: 60% of the D. melanogaster genome plays no role in differences between resistant and susceptible populations. Instead, resistance gene(s) are restricted to chromosome two, and may be further restricted to the centromeric region of this chromosome. This finding suggests that natural adaptations—like many responses to artificial selection and human disturbance—sometimes have a simple genetic basis.     

Hydrated electrons and prebiotic evolution

It is proposed that reactions of the hydrated electron e_aq^? in the “primordial soup” were an evolutionary pressure which selected biopolyelectrolytes, coacervates, “organelles” and lipid-membrane-bound structures of a pattern found in the biosphere today.The two physical restrictions of e_aq^? reactivity which determined its evolutionary specificity are (a) its exclusion from polyanion domains in Donman fashion, and (b) its inability to solvate in alkanes. Thus, (1) polyanions (as opposed to polyanions) and (2) lipid-membrane-bound (as opposed to free) structures are protected from e_aq^? reactivity and degradation. The polyanionic nature of the current biosphere, and the prevalence of anionic polyanion-polycation complexes (such as ribosomes and chromatin), are attributed to (1). (2) co-operated in protecting the products of (1) as salinity in the “primordial soup” increased and (a) was no longer important. The evolution of DNA, and the existence of electron transport mechanisms are seen as logical extensions of the properties of e_aq^? Experimental evidence is already available to support all the postulated processes.     

What is hierarchical selection?

It has been proposed that natural selection occurs on a hierarchy of levels, of which the organismic level is neither the top nor the bottom. This hypothesis leads to the following practical problem: in general, how does one tell if a given phenomenon is a result of selection on level X or level Y. How does one tell what the units of selection actually are? It is convenient to assume that a unit of selection may be defined as a type of entity for which there exists, among all entities on the same “level” as that entity, an additive component of variance for some specific component F of fitness which does not appear as an additive component of variance in any decomposition of this F among entities at any lower level. But such a definition implicitly assumes that if f(x, y) depends nonadditively on its arguments, there must be interaction between the quantities which x and y represent. This assumption is incorrect. And one cannot avoid this error by speaking of “transformability to additivity” instead of merely “additivity”. A general mathematical formulation of the concepts of interaction and non-interaction is proposed, followed by a correspondingly modified approach to the definition of a unit of selection. The practical difficulty of verifying the presence of hierarchical selection is discussed.     

Complex adaptive traits between mating behaviour and post-copulatory sperm behaviour in squids

Emergence of male dimorphism within a species is the evolutionary process of disruptive selection. In squids, two types of male mating behaviour, known as alternative reproductive tactics (ARTs), are causally associated with adult body size. Males inseminate promiscuously with the same females; large “consort” males internally, and small “sneaker” males externally. Previously we found that in Heterololigo bleekeri, sneaker (but not consort) spermatozoa are able to swarm by sensing self-emitted CO₂. This suggests that a swarming trait might have arisen in sneakers as a “sperm cooperation” strategy among sibling sperm in order to compete with consort males, or as a consequence of adaptation to external fertilization. To address these possibilities, we examined six species where three patterns of insemination are present, namely, only internal, only external, or both ARTs. In three species that employ both ARTs (H. bleekeri, Loligo reynaudii and Uroteuthis edulis), sneaker spermatozoa always exhibited self-swarming capacity. In Idiosepius paradoxus and Todarodes pacificus, which use only external insemination, spermatozoa formed a swarm. However, in Euprymna morsei, which use only internal insemination, sperm were unable to swarm. These results suggest that the self-swarming trait is likely to be linked to the mode of insemination rather than the alternative strategy used by sneaker males. Thus we propose a new hypothesis in which cooperative sperm behaviour has evolved not only through kin selection against sperm competition risks, but also through adaptation to the insemination/fertilization environment.     

Characterizing the Evolutionary Path(s) to Early Homo

Numerous studies suggest that the transition from Australopithecus to Homo was characterized by evolutionary innovation, resulting in the emergence and coexistence of a diversity of forms. However, the evolutionary processes necessary to drive such a transition have not been examined. Here, we apply statistical tests developed from quantitative evolutionary theory to assess whether morphological differences among late australopith and early Homo species in Africa have been shaped by natural selection. Where selection is demonstrated, we identify aspects of morphology that were most likely under selective pressure, and determine the nature (type, rate) of that selection. Results demonstrate that selection must be invoked to explain an Au. africanus—Au. sediba—Homo transition, while transitions from late australopiths to various early Homo species that exclude Au. sediba can be achieved through drift alone. Rate tests indicate that selection is largely directional, acting to rapidly differentiate these taxa. Reconstructions of patterns of directional selection needed to drive the Au. africanus—Au. sediba—Homo transition suggest that selection would have affected all regions of the skull. These results may indicate that an evolutionary path to Homo without Au. sediba is the simpler path and/or provide evidence that this pathway involved more reliance on cultural adaptations to cope with environmental change.     

Dissecting the Genetic Basis of a Complex cis-Regulatory Adaptation

Although single genes underlying several evolutionary adaptations have been identified, the genetic basis of complex, polygenic adaptations has been far more challenging to pinpoint. Here we report that the budding yeast Saccharomyces paradoxus has recently evolved resistance to citrinin, a naturally occurring mycotoxin. Applying a genome-wide test for selection on cis-regulation, we identified five genes involved in the citrinin response that are constitutively up-regulated in S. paradoxus. Four of these genes are necessary for resistance, and are also sufficient to increase the resistance of a sensitive strain when over-expressed. Moreover, cis-regulatory divergence in the promoters of these genes contributes to resistance, while exacting a cost in the absence of citrinin. Our results demonstrate how the subtle effects of individual regulatory elements can be combined, via natural selection, into a complex adaptation. Our approach can be applied to dissect the genetic basis of polygenic adaptations in a wide range of species.     

A Darwinian evolutionary system. 3. Experiments on the evolution of feeding patterns

Another application of the Darwinian evolutionary system introduced earlier is presented. The evolution of spiraling and meandering feeding patterns, as exemplified by the marine polychaete Paraonis fulgens, was simulated by constructing an artificial “worm”, called Rectangulus, because it was capable of turning around 90 ° only. The behavioural program of Rectangulus contained six parameters, which controlled the following properties: (i) turning spontaneously after a given number of steps, (ii) turning before a former track, (iii) avoiding entering a “channel”, i.e. a path flanked by former tracks, (iv) keeping contact with former tracks, (v) performing a turn at the beginning (which in combination with contact-keeping leads to a spiral), and (vi) switching from spiraling to meandering behaviour after a given number of steps. These parameters were binary-coded in the “genomes” of Rectangulus, and were capable of mutating and recombining.Evolutionary experiments were performed with populations consisting of 50 individuals, inhabiting an area of 100 × 100 “unit steps”. Each individual had to “forage” for 140 steps, and the number of successful (uncovered area) and unsuccessful (area covered previously) steps were recorded. Individuals with greater “yield” (successful minus unsuccessful steps, divided by the total number of steps) had a greater probability of being reproduced (selection). It was found that Rectangulus soon “learned” to turn in front of a former track and a channel, and to keep contact, both if one starts with individuals who at the beginning could only go straight ahead, or with ones turning after every step. Evolution from this stage onward proceeded more variably. Different types of meandering, spiraling, and a combination of both emerged; however, in two out of six cases, evolution did not proceed beyond the turning and contact-keeping stage. It is suggested that the different outcomes represent separate adaptive peaks. The highest yield was obtained by the combination of spiraling and meandering, as used by Paraonis fulgens, followed by pure spiraling and meandering. This was confirmed by calculations made for populations with fixed parameters. The results further show that selection for non-crossing could only have been effective in producing these patterns for population densities much higher than the ones found for P. fulgens at the present time.     

How to Rethink Evolutionary Theory: A Plurality of Evolutionary Patterns

Nature has recently depicted the empirical advancements of the theory of evolution as a confrontation between “reformists”, that claim for an urgent rethinking of the standard neo-Darwinian approach including so far neglected factors and processes, and “conservatives” who reply “all is well” about the current evolutionary research programme based on genetic variation and natural selection. The fight is mainly around genetic reductionism, but it seems inconclusive. Reformists stress very important factors, but they are still missing a coherent proposal about the architecture of the future extended evolutionary theory. Conservative react defensively, relying just on non-essential add-ons to the old and stable neo-Darwinian core. We analyze the debate and we propose an interpretation. Evolutionary biology is a rapidly expanding field. The bone of contention is how to update and extend the central core of the Darwinian legacy. We propose here the idea that what is happening in the field today is a development of the evolutionary research programme, whose structure is composed of a set of compatible and integrated evolutionary patterns. Evolutionary biology has been extended over its history by the inclusion of more and more patterns, rather than by revision to core theory. Niles Eldredge’s “Hierarchy Theory” is an example of global structure (meta-theory) aiming at incorporating and unifying the currently observed evolutionary patterns.     

Levels or Domains of Life?

In the case of living beings – the very concept of “level” of organization becomes obscure: it suggests a value-based assessment, assigning notions like “lower” and “higher” with rather vague criteria for constructing the ladder of perfection, complexity, importance, etc. We prefer therefore the term “domain”, entities ranking equal. Domains may represent natural entities as well as purely human constructs developed in order to gain understanding of some facets of living things; living, evolved beings (e.g. viviparous animals, eukaryotic cells, etc.) as well as those abstract constructs, such as genotype and ‘niche’ which have been developed in the search for better understanding of such living things. Delimitation of such domains is sometimes a question of the dexterity of the researcher, and sometimes draws from the tradition in a given field. Such domains are not completely (canonically) translatable to each other. Rather, they interact by a process that we call here reciprocal formation. Life (including the biosphere and human cultures which are emergent within the frame of the biosphere) is unique among multi-domain systems. In contrast to purely physical systems, life is a semiotic system driven by the historical experience of lineages, interpreted and re-interpreted by the incessant turnover of both individuals and their communities. This paper provides cases of domain interrelations, and addresses two questions: (1) How do new qualities of inter-domain interaction emerge historically? (2) How do new domains (ways of understanding the world) emerge in evolution. Two approaches, physical and biosemiotic, are discussed as we seek to get a better understanding of the overarching tasks.     

Darwin,the amphibians,and the natural selection

A critical review of Darwin's publications shows that he did not dissert much about amphibians, in comparison with the other tetrapods. However, in “A Naturalist's Voyage round the World”, Darwin described for the first time several amphibian species and was surprised by their peculiar way of life, terrestrial or euryhaline. These amphibian observations around the world led Darwin to discuss evolutionnary notions, like developmental heterochronies or evolving convergences, and later to illustrate his famous natural selection theory. This is confirmed, for example, by the publication of “On the Origin of Species” where Darwin ironically questioned creation theory, trying to explain the absence of amphibians on oceanic islands. Lamarck also considered amphibians as relevant material to illustrate his theory of acquired character heredity. These historical uses of lissamphibians as evolutionary models have been mostly realized before any amphibian fossil discovery, i.e. out of a palaeontological context.