Model selection in ecology and evolution

Recently, researchers in several areas of ecology and evolution have begun to change the way in which they analyze data and make biological inferences. Rather than the traditional null hypothesis testing approach, they have adopted an approach called model selection, in which several competing hypotheses are simultaneously confronted with data. Model selection can be used to identify a single best model, thus lending support to one particular hypothesis, or it can be used to make inferences based on weighted support from a complete set of competing models. Model selection is widely accepted and well developed in certain fields, most notably in molecular systematics and mark-recapture analysis. However, it is now gaining support in several other areas, from molecular evolution to landscape ecology. Here, we outline the steps of model selection and highlight several ways that it is now being implemented. By adopting this approach, researchers in ecology and evolution will find a valuable alternative to traditional null hypothesis testing, especially when more than one hypothesis is plausible.     

Ecologically relevant stress resistance: from microarrays and quantitative trait loci to candidate genes — A research plan and preliminary results using<Emphasis Type="Italic">Drosophila</Emphasis> as a model organism and climatic and genetic stress as model stresses

We aim at studying adaptation to genetic and environmental stress and its evolutionary implications at different levels of biological organization. Stress influences cellular processes, individual physiology, genetic variation at the population level, and the process of natural selection. To investigate these highly connected levels of stress effects, it is advisable - if not critical - to integrate approaches from ecology, evolution, physiology, molecular biology and genetics. To investigate the mechanisms of stress resistance, how resistance evolves, and what factors contribute to and constrain its evolution, we use the well-defined model systems ofDrosophila species, representing both cosmopolitan species such asD. melanogaster with a known genome map, and more specialized and ecologically well described species such as the cactophilicD. buzzatii. Various climate-related stresses are used as model stresses including desiccation, starvation, cold and heat. Genetic stress or genetic load is modelled by studying the consequences of inbreeding, the accumulation of (slightly) deleterious mutations, hybridization or the loss of genetic variability. We present here a research plan and preliminary results combining various approaches: molecular techniques such as microarrays, quantitative trait loci (QTL) analyses, quantitative PCR, ELISA or Western blotting are combined with population studies of resistance to climatic and genetic stress in natural populations collected across climatic gradients as well as in selection lines maintained in the laboratory.     

How scientists perceive the evolutionary origin of human traits: Results of a survey study

Various hypotheses have been proposed for why the traits distinguishing humans from other primates originally evolved, and any given trait may have been explained both as an adaptation to different environments and as a result of demands from social organization or sexual selection. To find out how popular the different explanations are among scientists, we carried out an online survey among authors of recent scientific papers in journals covering relevant fields of science (paleoanthropology, paleontology, ecology, evolution, human biology). Some of the hypotheses were clearly more popular among the 1,266 respondents than others, but none was universally accepted or rejected. Even the most popular of the hypotheses were assessed “very likely” by <50% of the respondents, but many traits had 1–3 hypotheses that were found at least moderately likely by >70% of the respondents. An ordination of the hypotheses identified two strong gradients. Along one gradient, the hypotheses were sorted by their popularity, measured by the average credibility score given by the respondents. The second gradient separated all hypotheses postulating adaptation to swimming or diving into their own group. The average credibility scores given for different subgroups of the hypotheses were not related to respondent's age or number of publications authored. However, (paleo)anthropologists were more critical of all hypotheses, and much more critical of the water‐related ones, than were respondents representing other fields of expertise. Although most respondents did not find the water‐related hypotheses likely, only a small minority found them unscientific. The most popular hypotheses were based on inherent drivers; that is, they assumed the evolution of a trait to have been triggered by the prior emergence of another human‐specific behavioral or morphological trait, but opinions differed as to which of the traits came first.     

What drives variation in the corticosterone stress response between subspecies? A common garden experiment of swamp sparrows (Melospiza georgiana)

Although differences in the corticosterone stress response have frequently been reported between populations or closely related subspecies, their origin remains unclear. These differences may appear because individuals adjust their corticosterone stress response to the environmental conditions they are experiencing. However, they may also result from selection that has favoured individuals with specific corticosterone stress response or from environmental factors that have affected the development of the corticosterone stress response during early life. We investigated these hypotheses by studying the corticosterone stress response of two closely related subspecies of swamp sparrows (Melospiza sp.). We showed for the first time that two closely related subspecies can differ in their corticosterone stress response when raised at the laboratory and held in similar conditions for a year. Thus, we demonstrated that selection, developmental processes or a conjunction of both of these processes can account for variation in the stress response between closely related subspecies.     

Conceptual issues in local adaptation

Studies of local adaptation provide important insights into the power of natural selection relative to gene flow and other evolutionary forces. They are a paradigm for testing evolutionary hypotheses about traits favoured by particular environmental factors. This paper is an attempt to summarize the conceptual framework for local adaptation studies. We first review theoretical work relevant for local adaptation. Then we discuss reciprocal transplant and common garden experiments designed to detect local adaptation in the pattern of deme × habitat interaction for fitness. Finally, we review research questions and approaches to studying the processes of local adaptation – divergent natural selection, dispersal and gene flow, and other processes affecting adaptive differentiation of local demes. We advocate multifaceted approaches to the study of local adaptation, and stress the need for experiments explicitly addressing hypotheses about the role of particular ecological and genetic factors that promote or hinder local adaptation. Experimental evolution of replicated populations in controlled spatially heterogeneous environments allow direct tests of such hypotheses, and thus would be a valuable way to complement research on natural populations.     

动物内温性进化研究进展

对动物内温性进化的研究进行了较为系统的论述,包括内温性动物概念的由来、特点和起源的选择因子。内温性起源的选择因子包括8个模型：热生态位扩展模型、恒温与代谢效率模型、降低个体大小模型、姿势改变模型、增加脑大小模型、有氧呼吸能力模型、双亲行为模型和同化能力模型。其中后3个模型较为重要。有氧呼吸能力模型认为,选择提高支持物理运动的最大呼吸能力,而增加的静止代谢作为其相关反应而得以进化。该假说得到种内研究数据的支持,而种问的数据并小完全支持。双亲行为模型是指在鸟兽类中,内温性是对双亲行为选择的结果,因为内温性为双亲控制抚育温度提供了保证。同化能力模型认为,在鸟类和兽类中内温性进化由以下两个因素所推动：①子代出生后双亲行为加强;②为支持每日总体能量高速消耗所需,动物内脏器官能力增强而导致的较高维持消耗。     

The species recognition hypothesis explains exaggerated structures in non-avialan dinosaurs better than sexual selection does

Several hypotheses have been proposed to explain “bizarre structures” in dinosaurs and other extinct animals (e.g., mechanical function and several kinds of intra- and interspecific display). Recent evidence and tests for species recognition as a possible driver of these structures have been proposed, in particular as an alternative to traditional hypotheses of function and sexual selection, which have fallen short. Advocates of sexual selection and mechanical function have advanced untested hypotheses claiming that species recognition cannot be an important process in evolution. We address these claims and show that they are based on misreading of the evidence and of previous literature. We also acknowledge that there have been historically differing definitions of sexual selection, which have greatly impeded understanding of the whole phenomenon of mate attraction and choice. Particularly in fossil animals, it is impossible to accept any hypothesis as the “default” that does not require evidence or testing to establish it.     

The evolution of gender-biased nectar production in hermaphroditic plants

The evolution of secondary sexual floral traits may be driven by selection through male or female reproductive success. Even so, the gender-biased function of a floral trait is often unapparent because secondary sexual traits and primary sexual organs of both genders co-occur within most bisexual flowers. Within dichogamous plants, however, secondary sexual traits may be unambiguously expressed in association with the primary sexual organs of one gender, making these species uniquely suited to studies of natural and sexual selection on floral traits. The objectives of this article are to summarize patterns of gender-biased nectar production and to critically explore theories relevant to its evolution. We list 41 species with gender-biased nectar production and provide two sets of adaptive hypotheses for the trait: sexual selection hypotheses and inbreeding avoidance hypotheses. We formulate these hypotheses using sexual selection theory in plants and the literature that relates pollinator foraging to plant inbreeding. We also consider explanations based on resource trade-offs, enemies, and genetic correlations. Support for the sexual selection and inbreeding avoidance hypotheses is provided by only a few well-studied species. We outline a series of experiments that should facilitate sorting among hypotheses. Plants with gender-biased nectar production are likely to provide unique insights into the roles of natural and sexual selection in the evolution of floral traits.     

The evolutionary origin of signa in female Lepidoptera: natural and sexual selection hypotheses

Signa are structures of the inner wall of the female corpus bursae (structure where males deposit a spermatophore during copulation) of many Lepidoptera that assist in tearing open spermatophores. In this paper, three hypotheses on the evolutionary origin of signa are proposed. The first hypothesis considers natural selection pressures arising from ecological changes that favor an increase in oviposition rate as the force behind the evolution of signa. The other two hypotheses involve sexual selection. The second hypothesis proposes that sexually antagonistic coevolution is responsible of the evolution of signa: According to this hypothesis, the inverse relation between the length of the female's refractory period and the amount of ejaculate remaining in her corpus bursae, observed in most Lepidoptera studied, selects in males a decreased rate of spermatophore digestion (e.g. a thicker spermatophore envelope or a higher chitin content) that increases the length of the refractory period beyond the female's optimum; in response, females evolved signa as a counteradaptation to restore the female's optimum by increasing the rate of spermatophore digestion. The last hypothesis considers that signa may have evolved as a female device for cryptic choice of males based on the ability of these to influence the length of post-copulatory female refractory period. The different hypotheses make different predictions of the sequence of appearance of specific ecological factors and novel phenotypic traits through evolutionary time. Therefore, testing the relative importance of the hypotheses requires a formal comparative analysis.     

Metabolic rates,genetic constraints,and the evolution of endothermy

The metabolic distinction between endotherms and ectotherms is profound. Whereas the ecology of metabolic rates is well studied, how endotherms evolved from their ectothermic ancestors remains unclear. The aerobic capacity model postulates that a genetic constraint between resting and maximal metabolism was essential for the evolution of endothermy. Using the multivariate breeders’ equation, I illustrate how the (i) relative sizes of genetic variances and (ii) relative magnitudes of selection gradients for resting and maximal metabolism affect the genetic correlation needed for endothermy to have evolved via a correlated response to selection. If genetic variances in existing populations are representative of ancestral conditions, then the aerobic capacity model is viable even if the genetic correlation was modest. The analyses reveal how contemporary data on selection and genetic architecture can be used to test hypotheses about the evolution of endothermy, and they show the benefits of explicitly linking physiology and quantitative genetic theory.     

DISENTANGLING THE EFFECTS OF KEY INNOVATIONS ON THE DIVERSIFICATION OF BROMELIOIDEAE (BROMELIACEAE)

The evolution of key innovations, novel traits that promote diversification, is often seen as major driver for the unequal distribution of species richness within the tree of life. In this study, we aim to determine the factors underlying the extraordinary radiation of the subfamily Bromelioideae, one of the most diverse clades among the neotropical plant family Bromeliaceae. Based on an extended molecular phylogenetic data set, we examine the effect of two putative key innovations, that is, the Crassulacean acid metabolism (CAM) and the water‐impounding tank, on speciation and extinction rates. To this aim, we develop a novel Bayesian implementation of the phylogenetic comparative method, binary state speciation and extinction, which enables hypotheses testing by Bayes factors and accommodates the uncertainty on model selection by Bayesian model averaging. Both CAM and tank habit were found to correlate with increased net diversification, thus fulfilling the criteria for key innovations. Our analyses further revealed that CAM photosynthesis is correlated with a twofold increase in speciation rate, whereas the evolution of the tank had primarily an effect on extinction rates that were found five times lower in tank‐forming lineages compared to tank‐less clades. These differences are discussed in the light of biogeography, ecology, and past climate change.     

SEXUAL DIMORPHISM,MATING SYSTEM AND BODY SIZE IN NEW WORLD BLACKBIRDS (ICTERINAE)

Although sexual selection is widely accepted as a primary functional cause of sexual size dimorphism in birds and mammals, results from some comparative studies have cast doubt on this conclusion. Chief among these contradictory results is the widespread association between body size and size dimorphism—large species tend to be more dimorphic than small species. This correlation is not directly predicted by the normal sexual selection scenario, and many hypotheses have been advanced to explain it. This paper reviews these hypotheses and evaluates them using data for the New World blackbirds (Icterinae). In this avian subfamily, (1) body size correlates with the intensity of sexual selection (as measured by mean harem size), and (2) size does not correlate with dimorphism if the effects of mating system are removed. Similar results are obtained when controlling for the confounding influence of phylogeny. Further, body size and mating system are associated with nesting dispersion. These results strongly argue that sexual dimorphism is a product of sexual selection in this subfamily, and suggest that either: (1) large body size itself, or the ecology of large species, promotes the development of coloniality and a polygynous mating system; or (2) polygyny and/or coloniality lead to the evolution of large size in both males and females. None of the other hypotheses examined predict an association between size and mating system, and all predict that size will correlate with dimorphism after the effects of mating system are removed. Thus, none of the other hypotheses seem applicable in this case. These results are compared to those obtained for other avian and mammalian taxa. Difficulties of analysis present in previous studies are discussed. I argue that it is inappropriate to assume that associations between a trait and body size or phylogeny are evidence of nonadaptive evolutionary “constraints.”     

The evolution and ecology of multiple antipredator defences

Prey seldom rely on a single type of antipredator defence, often using multiple defences to avoid predation. In many cases, selection in different contexts may favour the evolution of multiple defences in a prey. However, a prey may use multiple defences to protect itself during a single predator encounter. Such “defence portfolios” that defend prey against a single instance of predation are distributed across and within successive stages of the predation sequence (encounter, detection, identification, approach (attack), subjugation and consumption). We contend that at present, our understanding of defence portfolio evolution is incomplete, and seen from the fragmentary perspective of specific sensory systems (e.g., visual) or specific types of defences (especially aposematism). In this review, we aim to build a comprehensive framework for conceptualizing the evolution of multiple prey defences, beginning with hypotheses for the evolution of multiple defences in general, and defence portfolios in particular. We then examine idealized models of resource trade-offs and functional interactions between traits, along with evidence supporting them. We find that defence portfolios are constrained by resource allocation to other aspects of life history, as well as functional incompatibilities between different defences. We also find that selection is likely to favour combinations of defences that have synergistic effects on predator behaviour and prey survival. Next, we examine specific aspects of prey ecology, genetics and development, and predator cognition that modify the predictions of current hypotheses or introduce competing hypotheses. We outline schema for gathering data on the distribution of prey defences across species and geography, determining how multiple defences are produced, and testing the proximate mechanisms by which multiple prey defences impact predator behaviour. Adopting these approaches will strengthen our understanding of multiple defensive strategies.     

Chemical Ecology and Biomolecular Evolution

The belief in the Darwinian theory of evolution appeared to be shaken when one tried to interpret statements of molecular biology in it. As a consequence there arose a theory of non-Darwinian neutral evolution. The supporters of this theory believe that under natural conditions no factors exist which can distinguish and select organisms on their internal (molecular) structure. In the opinion of these neutralists natural selection cannot in principle control the molecular constitution of organisms. Contrary to the viewpoint of the critics of neutralism it is impossible to admit that nucleic acids, proteins and other biomolecules can evolve without the participation of natural selection. This controversy in contemporary theoretical biology can be solved by integrating the conceptions of molecular ecology with Darwinian theory. Molecular ecology acknowledges the interactions of organisms by means of chemical substances synthesized by them. Such chemical ecological factors play a leading part in the selective stages of biomolecular evolution. These diverse chemical ecological interrelations take place intensively when living beings interact with parasitic microbes.     

THE EVOLUTION OF REVERSED SEXUAL DIMORPHISM IN SIZE IN MONOGAMOUS SPECIES OF BIRDS

Reversed sexual dimorphism in size (RSD) occurs in most species of several taxonomic groups of birds. The hypotheses proposed to explain this phenomenon are examined theoretically, using inequalities to state selection in the most rigorous possible terms. The most pertinent empirical evidence is also examined critically. Proponents of hypotheses on the evolution of RSD have failed to consider the genetic constraints on the evolution of dimorphism. Selection for dimorphism can act on only that small portion of the genetic determination of body size that is sex limited. In general, selection for body size is much more likely to lead to a similar change (e.g. larger) in both sexes than to dimorphism. The most popular hypotheses involve selection for size-related differences in foraging ability. It is unlikely that there is variation in size-related foraging differences available for selection in a monomorphic, ancestral population. Foraging differences between the sexes cannot lead to the evolution of RSD; evolution of large and small morphs of both sexes is a more likely outcome. Selection for sex-role differentiation factors (e.g. large females lay larger eggs, small males are more agile in flight) can lead to the evolution of RSD, but only if the magnitudes of opposing selection for small males and for large females are equal. Combining selection for size-related foraging differences with selection for sex-role differentiation factors hinders the evolution of RSD until the sexes differ in size by 3 s.d . Empirical evidence supports this assertion: statistically significant differences between the sexes in the size of prey taken are found only in highly dimorphic species. The sex-role differentiation factors that have been proposed appear unlikely to provide the equal selection necessary for the evolution of RSD. Several authors have proposed that small size in males is selected for foraging ability and large size in females for some sex-role differentiation factor. Males cannot be more efficient foragers without females being less efficient and efficiency cannot be a factor only when the male is feeding his family. RSD cannot evolve in monogamous species if large females survive less well than small males. RSD might evolve as the result of sexual selection for small size in males and constraints on the reduction of size in females because of some factor associated with reproduction. Examination of seven studies indicating a relationship between female size and reproductive success shows very little unequivocal evidence for small size in females allowing breeding earlier in the season. Large size in females allows females to breed at a younger age in the sparrowhawk and pairs to form more rapidly in three species of sandpipers. Both of these may be the result of sexual selection. There are fewer theoretical problems with sexual selection as a cause for the evolution of RSD than with the other hypotheses. Empirical evidence for sexual selection is scarce but better than that for the other hypotheses. Evidence is contradictory for the selection of small size in males for agility in aerial displays for courtship or defence of territory. Large size in females does not appear to be the result of selection for competitive ability to obtain mates. Facilitation of female dominance and hence of the formation and maintenance of a pair bond is the most viable explanation of the evolution of RSD. It is most likely that all dimorphism (normal or reversed) is the result of sexual selection. RSD is correlated with birds in the diet in the Falconiformes and this is a central theme in the foraging hypotheses. This correlation may be because birds are abundant and available in a continuum of sizes, thus permitting but not causing the evolution of RSD or because species that prey upon birds are better equipped physically (and perhaps more likely behaviourally) to inflict damaging attacks on conspecifics and the greater RSD increases female dominance and the ease of pair formation.     

Habitat type and ambient temperature contribute to bill morphology

Avian bills are iconic structures for the study of ecology and evolution, with hypotheses about the morphological structure of bills dating back to Darwin. Several ecological and physiological hypotheses have been developed to explain the evolution of the morphology of bill shape. Here, we test some of these hypotheses such as the role of habitat, ambient temperature, body size, intraspecific competition, and ecological release on the evolution of bill morphology. Bill morphology and tarsus length were measured from museum specimens of yellow warblers, and grouped by habitat type, sex, and subspecies. We calculated the mean maximum daily temperature for the month of July, the hottest month for breeding specimens at each collecting location. Analysis of covariance models predicted total bill surface area as a function of sex, habitat type, body size, and temperature, and model selection techniques were used to select the best model. Habitat, mangrove forests compared with inland habitats, and climate had the largest effects on bill size. Coastal wetland habitats and island populations of yellow warblers had similar bill morphology, both of which are larger than mainland inland populations. Temperate but not tropical subspecies exhibited sexual dimorphism in bill morphology. Overall, this study provides evidence that multiple environmental factors, such as temperature and habitat, contribute to the evolution of bill morphology.     

The fitness of filamentous fungi

Fitness is a common currency in comparative biology. Without data on fitness, hypotheses about the adaptive significance of phenotypes or basic mechanisms of evolution, for example natural selection, remain speculative. Experiments with fungi can address questions specific to fungi or questions with a broader significance. Fungi can challenge the generality of fundamental evolutionary principles, yet there are no standard measures of fungal fitness. We argue that focusing on a single aspect of a complex life cycle, or a single measure of fitness (e.g. the number of asexual spores) is appropriate. Choosing which aspect of fitness to measure can be facilitated by an understanding of how fitness measures are correlated. Choices can also be based on the ecology of a species, for example whether a fungus is semelparous and reproduces once, or iteroparous and reproduces multiple times.     

GAMETE INTERACTIONS AND GENETIC DIFFERENTIATION AMONG THREE SYMPATRIC POLYCHAETES

The evolution of gamete incompatibility between free-spawning marine invertebrate species has been explained by three hypotheses: (1) independent divergence at gamete recognition loci; (2) selection against hybrids; and (3) a process of sexual selection involving polymorphic gamete recognition loci (Metz and Palumbi 1996). The first two hypotheses predict that gamete incompatibility appears only after gene flow has been halted for other reasons and the third that gamete incompatibility appears simultanously with blocks to gene flow. Here I show that gametes of three sympatric polychaetes in the genus Arctonoe are compatible in all crosses, over a broad range of gamete concentrations and contact times. Although at least some hybrid crosses produce fertile adults, allozyme and mitochondrial DNA sequence data indicate that the three species do not regularly exchange genes. These data are consistent with predictions of the first two hypotheses for the evolution of gamete incompatibility, but allow rejection of the third hypothesis. Gametes of the three species are compatible despite estimated divergence times of 1–3 M.Y.B.P.; in several other marine invertebrates, divergence times of the same magnitude are associated with asymmetric or complete gamete incompatibility. It appears likely that segregation of symbiotic adults on their respective host species restricts mating opportunities, and thus gene flow, among Arctonoe species.     

Longevity in Bovids Is Promoted by Sociality,But Reduced by Sexual Selection

Selection on intrinsic lifespan depends on both external factors affecting mortality and inherent tradeoffs in resource allocation between viability traits and other fitness-related traits. Longevity is therefore likely to vary between species in a sex-specific manner due to interspecific and intersexual differences in behavioural ecology. Here I focus on the bovid family to test two central hypotheses on longevity selection using the comparative method: firstly, that a reduction of extrinsic mortality in social species strengthens selection on intrinsic lifespan, and secondly, that mortality costs associated with intense sexual selection lead to shorter intrinsic lifespan. The results show that longevity (i) increases with sociality in both sexes and (ii) decreases with male-biased sexual size-dimorphism, but in males only. These discoveries suggest that sociality, a key ungulate strategy to reduce predation-related mortality, selects for inherently longer-lived organisms, and that strong sexual selection, which is known to compromise survival rates in the wild, can constrain also intrinsic lifespan. The contrasting results for males and females indicate that selection on longevity in the two sexes is partly uncoupled.