The Use of Functional and Adaptive Criteria in Phylogenetic Systematics

SYNOPSIS. The controversy over whether functional data can contributeto phylogenetic inference has grown in recent years. Steps canbe taken toward its resolution if the relevance of functionaldata is judged for each component of phylogenetic analysis.These components are (1)recognizing of basic taxa (species orsupraspecific taxa), (2) formulating hypotheses of homologyfollowed by character analysis, (3) evaluating character phylogeny,(4) formulating phylogenetic hypotheses, and (5) evaluatingalternative phylogenetic hypotheses. It can be shown that functionaldata do not play a necessary or unique role in any of thesecomponents of phylogenetic analysis. Arguments to the contraryhave failed to provide a rigorous, repeatable methodto incorporatefunctional data; proponents of a functional approach to phylogeneticreconstruction rely too often on subjective, authoritarian argumentation. Students of functional evolutionary morphology frequently havefailed to understand the kinds of information necessary to studyor apply the causal process of adaptation via natural selection.This information, required by the very nature of the theoryitself, includes knowing the pattern of heredity of the phenotypiccharacters being studied, relating intrapopulational phenotypicvariability to variation in fitness, and knowing a sufficientamount about population structure to specify the componentsof natural selection. Studies within functional evolutionarymorphology are not designed to satisfy these requirements. Functionalevolutionary morphology uses the concepts of adaptation andnatural selection axiomatically, and thus such studies contributenothing to our understanding of the evolutionary process becausehypotheses about that process are not being evaluated. Thisalso suggests that, if functional evolutionary morphology wishesto engage in analyses of the evolutionary dynamics of the phenotype,a reorientation of its research strategy and goals will be necessary.     

Adaptations and history

The historical definition of adaptations has come into wide use as comparative biologists have applied methods of phylogenetic analysis to a variety of evolutionary problems. Here we point out a number of difficulties in applying historical methods to the study of adaptation, especially in cases where a trait has arisen but once. In particular, the potential complexity of the genetic correlations among phenotypic traits, performance variables and fitness makes inferring past patterns of selection from comparative data difficult. A given pattern of character distribution may support many alternative hypotheses of mechanism. While phylogenetic data are limited in their ability to reveal evolutionary mechanisms, they have always been an important source of adaptive hypotheses and will continue to be so.     

Phylogeography and natural selection in the Tenerife gecko Tarentola delalandii: testing historical and adaptive hypotheses

Combining phylogeographic and matrix correspondence approaches in the analysis of geographical variation provides a fruitful approach to inferring the causes of molecular and morphological evolution within species. Here we present a study on the gecko Tarentola delalandii on the island of Tenerife, Canary Islands, which provides an outstanding model of an exceptionally high degree of phylogeographic differentiation in magnitude and pattern on a small spatial scale. We reconstruct the population history of T. delalandii using phylogeographic information, matrix correspondence tests and estimates of divergence times in conjunction with geological data. It appears that populations differentiated on three precursor islands and secondary contact followed the junction of these islands. The cytochrome b sequence appears to be evolving at least at approximately 1% per million years in this species. Matrix correspondence tests indicate that morphological character systems may reflect ecological selection regimes (colour pattern), history (body dimensions) or both (scalation). The results imply that natural selection can override a historical legacy, but also underline the potential relevance of molecular phylogenetic data for the interpretation of geographical variation in morphology.     

On adaptation, the assessment of adaptations, and the value of adaptive arguments in phylogenetic reconstruction

Evolutionary adaptation concerns a relative concept and the study of adaptations is directed to structures of individuals. The concept is devoid of any meaning when it is applied to species or populations. Adaptation is not synonymous with fitness or survival but does contribute to both of them. The term adaptation has a dual meaning since it refers both to the process of adaptation and to the state of being adapted. In the process of adaptation the mechanism of natural selection takes a prominent position. But the operation and effectiveness of natural selection are constrained by various limiting factors. Besides that, features may also be the result of nonadaptive evolution and only attain their present adaptive function at a later point in time. Another possibility is that features have at present a function different from the one for which they were initially designed. With respect to the state of being, the study of adaptation attempts to examine whether a particular feature indeed forms an adequate response to selection forces from the environment. Five methods or approaches generally are used to assess the adaptive significance of features, viz. the comparative, correlation, optimization, cladistic, and synthetic approach. Only the last-mentioned approach forms an adequate method since it attempts to establish, by direct analysis, which well-defined selection force exerts its influence on a certain character. The practicing taxonomist is faced with the problem that the data necessary to apply the synthetic method, generally require detailed field studies. Not all evolutionary changes are under the influence of natural selection. The presence of some features may be based on entirely different mechanisms, such as genetic drift, mutational pressure, pleiotropic gene action, allometric growth, or ecophenotypic responses. Various problems inherent to the optimization approach, and several others of practical and theoretical nature, make the morphocline method of the functional and evolutionary morphologists unsuitable as a method for phylogenetic reconstruction.     

Pleiotropic mutation, modularity and evolvability

The relationship between pleiotropy and the rate of evolution of a phenotypic character (evolvability) in a population is explored using computer simulations. I present results that suggest the rate of evolution of a phenotypic character may not decline when that character is pleiotropically associated to an increasing number of other characters, provided that the characters are under pure directional selection such that they are far from their optima relative to the average magnitude of a mutation. These conditions may be relevant during adaptive radiations. Adding pleiotropic associations to a set of characters in which one is under directional selection and the other is under stabilizing selection increases the rate of adaptation of the character under directional selection provided that the new characters that come to be pleiotropically associated are under directional selection. Thus, increasing the number of pleiotropic associations under these conditions increases the rate of adaptation of a character.     

Natural and artificial selection on a deviant character of the anal papillae in Drosophila melanogaster and their significance for salt adaptation

Artificial selection was carried out on a deviant character of remnants of the anal papillae in pupae of Drosophila melanogaster, i. e. stretched (S) instead of the normal retracted (R) papillae. A chromosomal interchange between the R- and S-selection lines revealed the polygenic determination of the S-character. A comparison of lines with a different number of chromosomes of the S-line shows the importance of properties of the anal papillae for salt adaptation. By a comparison of populations obtained by artificial selection for anal papillae and by natural selection for salt adaptation we could analyse the significance of the deviant character under natural selection on media with increasing percentages of salt. Our results shows that taking into account only one character in natural selection is often a simplification. However, applying artificial selection on components of the phenotype contributing to the adaptation make an important contribution to the analysis of adaptive processes.     

EXPERIMENTAL MANIPULATION OF PUTATIVE SELECTIVE AGENTS PROVIDES EVIDENCE FOR THE ROLE OF NATURAL ENEMIES IN THE EVOLUTION OF PLANT DEFENSE

Although biologists have long assumed that plant resistance characters evolved under selection exerted by such natural enemies as herbivores and pathogens, experimental evidence for this assumption is sparse. We present evidence that natural enemies exert selection on particular plant resistance characters. Specifically, we demonstrate that elimination of natural enemies from an experimental field population of Arabidopsis thaliana alters the pattern of selection on genetic variation in two characters that have been shown to reduce herbivore damage in the field: total glucosinolate concentration and trichome density. The change in pattern of selection reveals that natural enemies imposed selection favoring increased glucosinolate concentration and increased trichome density, and thus, supports one of the major assumptions of the coevolution hypothesis. We also demonstrate that a pattern of stabilizing selection on glucosinolate concentration results from a balance between the costs and benefits associated with increasing levels of this resistance character. This result provides direct confirmation of the appropriateness of cost-benefit models for characterizing the evolution of plant defenses.     

人工选择下旱地小麦生长塑性与产量形成特征

旱地小麦在进化过程中经受了自然和人工的双重选择,其中人工选择在品种驯化和改良过程中扮演了关键的角色.本文综述了人工选择下旱地小麦进化特征、生理可塑性、形态可塑性和种群属性演变等几个相对独立、但又相互联系的问题,探讨了旱地小麦适应逆境胁迫的生理生态机理,并勾画了其进化路线.在旱地小麦从二倍体到六倍体的漫长进化历程中,自然选择对小麦适应外界环境起到关键作用;随着人工选择的介入,以产量为主要目标的性状选择不断得到强化,从群体上呈现适应逆境的形态特征.人工选择下旱地小麦的水分及养分利用效率不断提升,生物量分配呈现出地下部减少、地上部增加的分配特征,对密度胁迫和高温胁迫的耐受性不断增强,但单位面积光合速率呈逐渐降低趋势.旱地小麦生产是复杂的群体过程,而非简单的个体反应.人工选择提高了旱地小麦的种群适合度和个体繁殖分配,强化了与环境的协同性,却弱化了其自然种群属性.本文还对旱地小麦的进化图进行了描绘,对气候变化下旱地小麦育种和栽培管理提出几点建议.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

CLINES IN CUTICULAR HYDROCARBONS IN TWO DROSOPHILA SPECIES WITH INDEPENDENT POPULATION HISTORIES

We took a comparative approach utilizing clines to investigate the extent to which natural selection may have shaped population divergence in cuticular hydrocarbons (CHCs) that are also under sexual selection in Drosophila. We detected the presence of CHC clines along a latitudinal gradient on the east coast of Australia in two fly species with independent phylogenetic and population histories, suggesting adaptation to shared abiotic factors. For both species, significant associations were detected between clinal variation in CHCs and temperature variation along the gradient, suggesting temperature maxima as a candidate abiotic factor shaping CHC variation among populations. However, rainfall and humidity correlated with CHC variation to differing extents in the two species, suggesting that response to these abiotic factors may vary in a species‐specific manner. Our results suggest that natural selection, in addition to sexual selection, plays a significant role in structuring among‐population variation in sexually selected traits in Drosophila.     

Evolution of Functional Genes in Cetaceans Driven by Natural Selection on a Phylogenetic and Population Level

Cetaceans represent an evolutionary lineage marked by drastic morphological and physiological changes during their adaptation to an exclusively marine existence. In addition, several cetacean species exhibit geographical ranges that encompass different marine environments, with genetic breaks being sometimes consistent with environmental breaks. As such, genes that underwent adaptation during the land-sea transition can also be potential candidates for adaptation to different oceanic environments. In this study, we analysed 3 milk protein genes (β-casein, κ-casein, and α-lactalbumin) and 2 immunity related genes (MHC DQβ1 and γ-fibrinogen) for selection based on available phylogenetic datasets of both mammals and cetaceans, and used the results from this analysis to assess adaptation to different environments on a population level in the European common dolphin (Delphinus delphis). We found that evidence for positive selection could be detected in all genes in the phylogenetic analyses, with β-casein showing a further increase in selective pressure in the cetacean lineage. At the population level, both the immune system locus DQβ1 and β-casein genes showed patterns of variation consistent with divergent selection, and in each case the same populations showed differentiation. One of these populations was also differentiated at neutral markers, while the other was not. We discuss possible inference, and the potential for the further development of these ideas using genomic technologies.     

Morphological vs. molecular evolution: ecology and phylogeny both shape the mandible of rodents

What actually is the expected pattern relating to molecular and morphological divergence? A phylogenetic correlation is expected; however, natural selection may force morphological evolution away from this expected correlation. To assess this relationship and the way it is modulated by selection, we investigated the radiation of the murine rodents, also called as Old World rats and mice. Regarding their diet, they are diversified as they include many omnivorous as well as specialist taxa. The size and shape of the mandible, a morphological character involved in the feeding process, was quantified and compared with an estimate of molecular divergence based on interphotoreceptor retinoid binding protein (IRBP) sequences. Size and shape of the mandible appeared to be related by an allometric relationship whatever the ecology of the taxa. Small size characterizes most murines, causing a dominance of low size distances; still, the frequency of important size differentiation increases with molecular distances. Regarding shape changes, the pattern is much contrasted between omnivores and specialists. A pattern of phenotypic drift characterizes the mandible evolution of taxa sharing an omnivorous diet. Little saturation occurs over more than 10 million years with regard to the shape of the mandible that appears as a valuable marker of phylogenetic history in this context. In contrast, important morphological distances can occur when specialist taxa are involved, even when the molecular divergence is small. Ecological specialization thus triggers an uncoupling of molecular and phenotypic evolution, and the departure from a phenotypic drift pattern.     

GENETIC CONSTRAINTS ON ADAPTATION TO A CHANGING ENVIRONMENT

Genetic correlations between traits can constrain responses to natural selection. To what extent such correlations limit adaptation depends on patterns of directional selection. I derive the expected rate of adaptation (or evolvability) under randomly changing selection gradients. When directional selection gradients have an arbitrary covariance matrix, the average rate of adaptation depends on genetic correlations between traits, contrary to the isotropic case investigated in previous studies. Adaptation may be faster on average with more genetic correlation between traits, if these traits are selected to change jointly more often than the average pair of traits. However, natural selection maximizes the long‐term fitness of a population, not necessarily its rate of adaptation. I therefore derive the average lag load caused by deviations of the mean phenotype from an optimum, under several forms of environmental changes typically experienced by natural populations, both stochastic and deterministic. Simple formulas are produced for how the G matrix affects long‐term fitness in these contexts, and I discuss how their parameters can be estimated empirically.     

Quantitative genetic variability maintained by mutation-stabilizing selection balance: sampling variation and response to subsequent directional selection

A model of genetic variation of a quantitative character subject to the simultaneous effects of mutation, selection and drift is investigated. Predictions are obtained for the variance of the genetic variance among independent lines at equilibrium with stabilizing selection. These indicate that the coefficient of variation of the genetic variance among lines is relatively insensitive to the strength of stabilizing selection on the character. The effects on the genetic variance of a change of mode of selection from stabilizing to directional selection are investigated. This is intended to model directional selection of a character in a sample of individuals from a natural or long-established cage population. The pattern of change of variance from directional selection is strongly influenced by the strengths of selection at individual loci in relation to effective population size before and after the change of regime. Patterns of change of variance and selection responses from Monte Carlo simulation are compared to selection responses observed in experiments. These indicate that changes in variance with directional selection are not very different from those due to drift alone in the experiments, and do not necessarily give information on the presence of stabilizing selection or its strength.     

Population Genetic Studies Revealed Local Adaptation in a High Gene-Flow Marine Fish,the Small Yellow Croaker (Larimichthys polyactis)

The genetic differentiation of many marine fish species is low. Yet local adaptation may be common in marine fish species as the vast and changing marine environment provides more chances for natural selection. Here, we used anonymous as well as known protein gene linked microsatellites and mitochondrial DNA to detect the population structure of the small yellow croaker (Larimichthys polyactis) in the Northwest Pacific marginal seas. Among these loci, we detected at least two microsatellites, anonymous H16 and HSP27 to be clearly under diversifying selection in outlier tests. Sequence cloning and analysis revealed that H16 was located in the intron of BAHCC1 gene. Landscape genetic analysis showed that H16 mutations were significantly associated with temperature, which further supported the diversifying selection at this locus. These marker types presented different patterns of population structure: (i) mitochondrial DNA phylogeny showed no evidence of genetic divergence and demonstrated only one glacial linage; (ii) population differentiation using putatively neutral microsatellites presented a pattern of high gene flow in the L. polyactis. In addition, several genetic barriers were identified; (iii) the population differentiation pattern revealed by loci under diversifying selection was rather different from that revealed by putatively neutral loci. The results above suggest local adaptation in the small yellow croaker. In summary, population genetic studies based on different marker types disentangle the effects of demographic history, migration, genetic drift and local adaptation on population structure and also provide valuable new insights for the design of management strategies in L. polyactis.     

Adaptation and functional integration in primate phylogenetics

In two areas of phylogenetics, contrary predictions have been developed and maintained for character analysis and weighting. With regard to adaptation, many have argued that adaptive characters are poorly suited to phylogenetic analysis because of a propensity for homoplasy, while others have argued that complex adaptive characters should be given high weight because homoplasy in complex characters is unlikely. Similarly, with regard to correlated sets of characters, one point of view is that such sets should be collapsed into a single character-a single piece of phylogenetic evidence. Another point of view is that a suite of correlated characters should be emphasized in phylogenetics, again because recurrence of detailed similarity in the same suite of features is unlikely. In this paper, I discuss the theoretical background of adaptation and functional integration with respect to phylogenetic systematics of primates. Several character examples are reviewed with regard to their functional morphology and phylogenetic signal: postorbital structures, tympanic morphology, fusion of the mandibular symphysis, the tooth comb, strepsirrhine talar morphology, and the prehensile tail. It is clear when considering characters such as these that some characters are synapomorphic of major clades and at the same time functionally important. This appears particularly to be the case when characters are integrated into a complex and maintained as stable configurations. Rather than being simply a problem in character analysis, processes of integration may help to explain the utility of phylogenetically informative characters. On the other hand, the character examples also highlight the difficulty in forming a priori predictions about a character's phylogenetic signal. Explanations of patterns of character evolution are often clade-specific, which does not allow for a simple framework of character selection and/or weighting.     

Comparison of phylogenetic signal between male genitalia and non-genital characters in insect systematics

It is generally accepted that male genitalia evolve more rapidly and divergently relative to non-genital traits due to sexual selection, but there is little quantitative comparison of the pattern of evolution between these character sets. Moreover, despite the fact that genitalia are still among the most widely used characters in insect systematics, there is an idea that the rate of evolution is too rapid for genital characters to be useful in forming clades. Based on standard measures of fit used in cladistic analyses, we compare levels of homoplasy and synapomorphy between genital and non-genital characters of published data sets and demonstrate that phylogenetic signal between these two character sets is statistically similar. This pattern is found consistently across different insect orders at different taxonomic hierarchical levels. We argue that the fact that male genitalia are under sexual selection and thus diverge rapidly does not necessarily equate with the lack of phylogenetic signal, because characters that evolve by descent with modification make appropriate characters for a phylogenetic analysis, regardless of the rate of evolution. We conclude that male genitalia are a composite character consisting of different components diverging separately, which make them ideal characters for phylogenetic analyses, providing information for resolving varying levels of hierarchy.
© The Willi Hennig Society 2009.     

Between-host evolution of cytotoxic T-lymphocyte epitopes in human immunodeficiency virus type 1: an approach based on phylogenetically independent comparisons

In human immunodeficiency virus type 1 (HIV-1), mutations that escape from cytotoxic T-lymphocyte (CTL) recognition have been documented, and sequence analyses have provided indirect support for the hypothesis that natural selection has favored CTL escape mutants within an infected host. In spite of such evidence for within-host selection by CTL, it has been more difficult to determine how natural selection by host CTL has influenced long-term evolution of HIV-1. We used statistical analysis of published HIV-1 genomic sequences to examine the role of natural selection in between-host evolution of CTL epitopes. Based on a phylogenetic analysis, we identified 21 pairs of closely related genomes isolated from different hosts and examined the pattern of nucleotide substitution in genomic regions encoding well-characterized CTL epitopes. The results revealed that certain CTL epitopes have been subject to repeated positive selection across the population, while others are generally conserved. Furthermore, evidence of positive selection was associated with divergence from the canonical epitope sequence and with an enhanced frequency of convergent amino acid sequence changes in CTL epitopes. The results support the hypothesis that CTL-driven selection has been a major factor in the long-term evolution of HIV-1.     

Sexual selection and ecological generalism are correlated in antbirds

Sexual selection is thought to counteract natural selection on the grounds that secondary sexual traits are inherently costly and evolve at the expense of naturally selected traits. It is therefore commonly predicted that increased sexual selection is associated with decreased physiological tolerance or ecological plasticity. Using phylogenetic comparative methods, we test this prediction by exploring relationships between traits assumed to be sexually selected (plumage dichromatism and song structure) and traits assumed to be naturally selected (altitudinal range and habitat range) in a diverse family of tropical birds. Contrary to expectations, we find that taxa with higher levels of dichromatism, and lower song pitch, occupy a wider variety of habitats and elevations. In other words, indices of sexual selection are positively related to two standard measures of ecological generalism. One interpretation of this pattern is that sexual selection combines synergistically with natural selection, thereby increasing physiological tolerance or the propensity to adapt to novel environments. An alternative possibility is that ecological generalism increases population density, which in turn promotes sexual selection in the form of greater competition for mates. Overall, our results suggest that a synergism between natural selection and sexual selection may be widespread, but the processes underlying this pattern remain to be investigated.