Function and organization: comparing the mechanisms of protein synthesis and natural selection

In this paper, we compare the mechanisms of protein synthesis and natural selection. We identify three core elements of mechanistic explanation: functional individuation, hierarchical nestedness or decomposition, and organization. These are now well understood elements of mechanistic explanation in fields such as protein synthesis, and widely accepted in the mechanisms literature. But Skipper and Millstein have argued (2005) that natural selection is neither decomposable nor organized. This would mean that much of the current mechanisms literature does not apply to the mechanism of natural selection. We take each element of mechanistic explanation in turn. Having appreciated the importance of functional individuation, we show how decomposition and organization should be better understood in these terms. We thereby show that mechanistic explanation by protein synthesis and natural selection are more closely analogous than they appear--both possess all three of these core elements of a mechanism widely recognized in the mechanisms literature.     

Three kinds of new mechanism

I distinguish three theses associated with the new mechanistic philosophy—concerning causation, explanation and scientific methodology. Advocates of each thesis are identified and relationships among them are outlined. I then look at some recent work on natural selection and mechanisms. Framing that debate in terms of different kinds of New Mechanism significantly affects what is at stake.     

Explanatory unification and natural selection explanations

The debate between the dynamical and the statistical interpretations of natural selection is centred on the question of whether all explanations that employ the concepts of natural selection and drift are reducible to causal explanations. The proponents of the statistical interpretation answer negatively, but insist on the fact that selection/drift arguments are explanatory. However, they remain unclear on where the explanatory power comes from. The proponents of the dynamical interpretation answer positively and try to reduce selection/drift arguments to some of the most prominent accounts of causal explanation. In turn, they face the criticism raised by statisticalists that current accounts of causation have to be violated in some of their core conditions or otherwise used in a very loose manner in order to account for selection/drift explanations. We propose a reconciliation of both interpretations by conveying evolutionary explanations within the unificationist model of scientific explanation. Therefore, we argue that the explanatory power in natural selection arguments is a result of successful unification of individual- and population-level facts. A short case study based on research on sympatric speciation will be presented as an example of how population- and individual-level facts are unified to explain the morphological mosaic of bill shape in island scrub jays (Aphelocoma insularis).     

Phenotypic selection on leaf water use efficiency and related ecophysiological traits for natural populations of desert sunflowers

Plant water-use efficiency (WUE) is expected to affect plant fitness and thus be under natural selection in arid habitats. Although many natural population studies have assessed plant WUE, only a few related WUE to fitness. The further determination of whether selection on WUE is direct or indirect through functionally related traits has yielded no consistent results. For natural populations of two desert annual sunflowers, Helianthus anomalus and H. deserticola, we used phenotypic selection analysis with vegetative biomass as the proxy for fitness to test (1) whether there was direct and indirect selection on WUE (carbon isotope ratio) and related traits (leaf N, area, succulence) and (2) whether direct selection was consistent with hypothesized drought/dehydration escape and avoidance strategies. There was direct selection for lower WUE in mesic and dry H. anomalus populations, consistent with dehydration escape, even though it is the longer lived of the two species. For mesic H. anomalus, direct selection favored lower WUE and higher N, suggesting that plants may be “wasting water” to increase N delivery via the transpiration stream. For the shorter lived H. deserticola in the direr habitat, there was indirect selection for lower WUE, inconsistent with drought escape. There was also direct selection for higher leaf N, succulence and leaf size. There was no direct selection for higher WUE consistent with dehydration avoidance in either species. Thus, in these natural populations of two desert dune species higher fitness was associated with some combination direct and indirect selection for lower WUE, higher leaf N and larger leaf size. Our understanding of the adaptive value of plant ecophysiological traits will benefit from further consideration of related traits such as leaf nitrogen and more tests in natural populations.     

Space,sympatry and speciation

Sympatric speciation remains controversial. ‘Sympatry’ originally meant “in the same geographical area”. Recently, evolutionists have redefined ‘sympatric speciation’ non‐spatially to require panmixia (m = 0.5) between a pair of demes before onset of reproductive isolation. Although panmixia is a suitable starting point in models of speciation, it is not a useful definition of sympatry in natural populations, because it becomes virtually impossible to find or demonstrate sympatry in nature. The newer, non‐spatial definition fails to address the classical debate about whether natural selection within a geographic overlap regularly causes speciation in nature, or whether complete geographic isolation is usually required. We therefore propose a more precise spatial definition by incorporating the population genetics of dispersal (or ‘cruising range’). Sympatric speciation is considerably more likely under this spatial definition than under the demic definition, because distance itself has a powerful structuring effect, even over small spatial scales comparable to dispersal. Ecological adaptation in two‐dimensional space often acts as a ‘magic trait’ that causes pleiotropic reductions of gene flow. We provide examples from our own research.     

Maintenance of handedness polymorphism in humans: a frequency-dependent selection model

Frequency-dependent selection is an important process in the maintenance of genetic variation in fitness. In humans, it has been proposed that the polymorphism of handedness is maintained by negative frequency-dependent selection, through a strategic advantage of left-handers in fighting interactions. Using simple mathematical models, we explore: (1) whether it is possible to predict the range of left-handedness frequencies observed in human populations by the frequency and the violence of fighting interactions; (2) the consequences of the sex differences in the probability of transmission of hand preference to offspring. We show that a wide range of values of the frequency of left-handers can be obtained with realistic changes of the parameters values. Our models reinforce the idea that negative frequency-dependence may have played a role in maintaining left-handedness in human populations, and provide further support for the importance of fighting interactions in the evolution of hand preference. Moreover, they suggest an explanation for the occurrence of left-handedness among women in this context, namely an indirect selective advantage through their male offspring.     

The Structure of Evolution by Natural Selection

We attempt a conclusive resolution of the debate over whether the principle of natural selection (PNS), especially conceived as the `principle' of the `survival of the fittest', is a tautology. This debate has been largely ignored for the past 15 years but not, we think, because it has actually been settled. We begin by describing the tautology objection, and situating the problem in the philosophical and biology literature. We then demonstrate the inadequacy of six prima facie plausible reasons for believing that the tautology debate has been satisfactorily resolved (the PNS is strictly a methodological principle; scientific theories can contain tautologies; the scope of the PNS has been reduced; theories should be understood as models and not exceptionless laws; the widespread acceptance of the propensity interpretation of fitness; and the abandonment of operationalism and verificationism). We proceed to a detailed discussion of Brandon's law (D) describing the PNS, and show that law (D) seriously misrepresents the structure of evolution by natural selection. In the final sections, we provide and defend a novel reinterpretation of the structure of the principle (or, we prefer, model) of evolution by natural selection.     

Multivariate phenotypes and the potential for alternative phenotypic optima in wall lizard (Podarcis muralis) ventral colour morphs

A major goal in evolutionary biology is to determine how phenotypic variation arises and is maintained in natural populations. Recent studies examining the morphological, physiological and behavioural differences among discrete colour morphotypes (morphs) have revealed several mechanisms that maintain discrete variation within populations, including frequency‐dependence, density‐dependence and correlational selection. For example, trade‐offs over resource allocation to morphological, physiological and behavioural traits can drive correlational selection for morph‐specific phenotypic optima. Here, we describe a ventral colour polymorphism in the wall lizard (Podarcis muralis) and test the hypothesis that morphs differ along multivariate axes defined by trade‐offs in morphological, physiological, and immunological traits. We show that ventral colour is a discrete trait and that morphs differ in body size, prevalence of infection by parasites and infection intensity. We also find that morphs differ along multivariate phenotypic axes and experience different multivariate selection pressures. Our results suggest that multivariate selection pressures may favour alternative optimal morph‐specific phenotypes in P. muralis.     

Conditions for the Maintenance of Prezygotic and Zygotic Isolation in a Continent-Island Model

A continent-island model is studied in which differences are initially present at a gene locus with assortative mating (which causes prezygotic reproductive isolation) and at one or two unlinked selected loci, (which cause zygotic reproductive isolation). This model simulates secondary contact between two populations which have diverged allopatrically at loci which control isolating mechanisms. Two different models of prezygotic isolation and three different models of zygotic isolation are studied. The analysis is focused on those conditions under which differentiation is not lost through the swamping effect of gene now. In each case the critical migration rate (m_c) below which differences can be maintained is found. Results depend on the degree of assortative mating, on the level of selection on the genes involved, and on the particular models of reproductive isolation considered. However, in all the models, for high values of such parameters the two isolating mechanisms interact strongly, and consequently the stability of the difference at each locus (as measured by m_c) is noticeably influenced by the presence of the difference at the other locus (or loci). The nature and strength of the effects of this interaction differ according to whether or not there is selection on the assortative mating locus and whether selection against hybrids or directional selection is hypothesized.     

Size-structure-based models of forest dynamics to interpret population- and community-level mechanisms

Functional size-structure-based models of forest tree population dynamics present a unifying explanation for population-level patterns and tree community organization. Density-dependent regulation can be explicitly replaced by the effect of size-structure-dependent suppression on demographic processes in functional size-structure models. This suppression effect sufficiently explains various patterns reported for crowded evenaged populations. Further, it stabilizes natural forest populations of overlapping generations at a stationary state with balanced recruitment and mortality. The spatial heterogeneity of light resources created by tree size structure offers an opportunity for multiple species to coexist by means of trade-offs between demographic parameters. The energy correlation of tree species diversity at a geographic scale is also attributable to the architectural feature of forests. Recipient of the Botanical Society Award of Young Scientists, 1992.     

SPATIAL VARIATION IN SELECTIVE REGIMES: SEXUAL SELECTION IN THE WATER STRIDER,GERRIS ODONTOGASTER

Studies of phenotypic selection in natural populations are often concerned with simply detecting selection. In adopting a more mechanistic approach, this study compares the sexual selection regimes in natural populations of the water strider Gerris odontogaster with a priori predictions of selection, based on a number of previous field and laboratory studies of the behavioral mechanisms of selection. In this species, a general reluctance of females to mate allows for intersexual selection for ability to subdue reluctant females in males. Female reluctance to mate has been shown to decrease with increasing population density, suggesting that sexual selection should be weaker in high density populations. Three different populations with large differences in population density were studied. A number of traits including parasite load, body mass, body size and male abdominal process length were found to experience significant sexual selection. The investigated populations differed considerably with regard to the total strength of selection on the measured traits and the form of selection on single traits. In general, males in the population with the highest density experienced the weakest selection for grasping ability. This pattern is ascribed to density-related alterations of female mating behavior. Selection for male grasping ability, as reflected by selection on male abdominal process length, is reduced in high-density populations where reluctant females are more easily subdued. Further, the studied populations differed significantly in mean phenotype and phenotypic variance for male abdominal process length. It is suggested that interpopulational differences in selective regimes may generate local adaptations with respect to male abdominal process length, and that gene flow may contribute to the maintenance of the high genetic variation in this trait. It is further suggested that more empirical effort should be made in quantifying and understanding spatial and temporal variation in selection in natural populations, since this may provide information on the prevalence of local adaptations in metric traits and on the mechanisms of selection.     

Clonal diversity driven by parasitism in a freshwater snail

One explanation for the widespread abundance of sexual reproduction is the advantage that genetically diverse sexual lineages have under strong pressure from virulent coevolving parasites. Such parasites are believed to track common asexual host genotypes, resulting in negative frequency‐dependent selection that counterbalances the population growth‐rate advantage of asexuals in comparison with sexuals. In the face of genetically diverse asexual lineages, this advantage of sexual reproduction might be eroded, and instead sexual populations would be replaced by diverse assemblages of clonal lineages. We investigated whether parasite‐mediated selection promotes clonal diversity in 22 natural populations of the freshwater snail Melanoides tuberculata. We found that infection prevalence explains the observed variation in the clonal diversity of M. tuberculata populations, whereas no such relationship was found between infection prevalence and male frequency. Clonal diversity and male frequency were independent of snail population density. Incorporating ecological factors such as presence/absence of fish, habitat geography and habitat type did not improve the predictive power of regression models. Approximately 11% of the clonal snail genotypes were shared among 2–4 populations, creating a web of 17 interconnected populations. Taken together, our study suggests that parasite‐mediated selection coupled with host dispersal ecology promotes clonal diversity. This, in return, may erode the advantage of sexual reproduction in M. tuberculata populations.     

Developmental matching and the numerical matching hypothesis for neuronal cell death

The nervous system contains some of the most precisely matching cell populations in an organism. It appears that a variety of ontogenetic buffer mechanisms ensure that precise matching develops reproducibly in all nervous systems. Selective cell death—one such neural ontogenetic buffer mechanism—operates by natural selection. Our mathematical model of matching by natural selection allows a detailed analysis of Hamburger's (1975) unique neuronal cell counts for the chick limb motor systems. We conclude that the numerical matching hypothesis is not a sufficient explanation for neuronal cell death—i.e., the excess neurons of the chick spinal motor column must have an additional developmental role besides ensuring numerical parity in the final neuro-muscular matching populations.     

Distinguishing Drift and Selection Empirically: “The Great Snail Debate” of the 1950s

Biologists and philosophers have been extremely pessimistic about the possibility of demonstrating random drift in nature, particularly when it comes to distinguishing random drift from natural selection. However, examination of a historical case – Maxime Lamotte’s study of natural populations of the land snail, Cepaea nemoralis in the 1950s – shows that while some pessimism is warranted, it has been overstated. Indeed, by describing a unique signature for drift and showing that this signature obtained in the populations under study, Lamotte was able to make a good case for a significant role for␣drift. It may be difficult to disentangle the causes of drift and selection acting in a population, but it is not (always) impossible.     

Impact of polymorphic transposable elements on linkage disequilibrium along chromosomes

Recombination and selection drive the extent of linkage disequilibrium (LD) among loci and therefore affect the reshuffling of adaptive genetic variation. However, it is poorly known to what extent the enrichment of transposable elements (TEs) in recombinationally‐inert regions reflects their inefficient removal by purifying selection and whether the presence of polymorphic TEs can modify the local recombination rate. In this study, we investigate how TEs and recombination interact at fine scale along chromosomes and possibly support linked selection in natural populations. Whole‐genome sequencing data of 304 individuals from nearby alpine populations of Arabis alpina were used to show that the density of polymorphic TEs is specifically correlated with local LD along chromosomes. Consistent with TEs modifying recombination, the characterization of 28 such LD blocks of up to 5.5 Mb in length revealed strong evidence of selective sweeps at a few loci through either site frequency spectrum or haplotype structure. A majority of these blocks were enriched in genes related to ecologically relevant functions such as responses to cold, salt stress or photoperiodism. In particular, the S‐locus (i.e., supergene responsible for strict outcrossing) was identified in a LD block with high levels of polymorphic TEs and evidence of selection. Another such LD block was enriched in cold‐responding genes and presented evidence of adaptive loci related to photoperiodism and flowering being increasingly linked by polymorphic TEs. These results are consistent with the hypothesis that TEs modify recombination landscapes and thus interact with selection in driving blocks of linked adaptive loci in natural populations.     

The genetic architecture of disease resistance in plants and the maintenance of recombination by parasites

Parasites represent strong selection on host populations because they are ubiquitous and can drastically reduce host fitness. It has been hypothesized that parasite selection could explain the widespread occurrence of recombination because it is a coevolving force that favours new genetic combinations in the host. A review of deterministic models for the maintenance of recombination reveals that for recombination to be favoured, multiple genes that interact with each other must be under selection. To evaluate whether parasite selection can explain the maintenance of recombination, we review 85 studies that investigated the genetic architecture of plant disease resistance and discuss whether they conform to the requirements that emerge from theoretical models. General characteristics of disease resistance in plants and problems in evaluating resistance experimentally are also discussed. We found strong evidence that disease resistance in plants is determined by multiple loci. Furthermore, in most cases where loci were tested for interactions, epistasis between loci that affect resistance was found. However, we found weak support for the idea that specific allelic combinations determine resistance to different host genotypes and there was little data on whether epistasis between resistance genes is negative or positive. Thus, the current data indicate that it is possible that parasite selection can favour recombination, but more studies in natural populations that specifically address the nature of the interactions between resistance genes are necessary. The data summarized here suggest that disease resistance is a complex trait and that environmental effects and fitness trade-offs should be considered in future models of the coevolutionary dynamics of host and parasites.     

Difference mechanisms: explaining variation with mechanisms

Philosophers of science have developed an account of causal-mechanical explanation that captures regularity, but this account neglects variation. In this article I amend the philosophy of mechanisms to capture variation. The task is to explicate the relationship between regular causal mechanisms responsible for individual development and causes of variation responsible for variation in populations. As it turns out, disputes over this relationship have rested at the heart of the nature–nurture debate. Thus, an explication of the relationship between regular causal mechanisms and causes of variation and between individual development and variation offers both the necessary amendment to the philosophy of mechanisms and the resources to mediate the dispute.     

Population-level variation of digestive physiology costs of mounting an immune response in damselflies

1. Trade-offs are often predicted to occur between energetically costly activities, such as somatic growth and eliciting immune responses to parasites. Although parasitism frequently reduces growth via lowered consumption, it remains unclear if the energetic demands of generating immune responses also affect the digestive physiological processes necessary for growth. Moreover, as local environmental conditions affect energetic investment towards growth and immune responses, the extent of any digestive–immune response trade-offs may vary among populations and not be fixed at the species-level. 2. To test these ideas, melanisation – a general innate immune response – was first induced in damselfly larvae (Enallagma vesperum) from two populations. The study then quantified growth and consumption rates, assimilation and production efficiencies, and daily metabolic rates to determine if digestive–immune response trade-offs were present and, if so, whether they differed between populations. 3. There was no evidence of any trade-offs between immune responses and digestive physiology components in either population. However, the results did show that populations differentially allocated energy towards different digestive physiology components after an immune response was elicited: one population increased their relative consumption and daily metabolic rates, while the other population had lower assimilation efficiencies and consumption rates. 4. Although researchers lack a mechanistic understanding of the observed population-level differences, these results suggest that accounting for population-level variation in digestive physiology and immune responses is critical to inferences about how immunological defences to parasitism may affect the ability for organisms to both acquire and utilise resources.