Multiple Explanations in Darwinian Evolutionary Theory

Variational evolutionary theory as advocated by Darwin is not a single theory, but a bundle of related but independent theories, namely: (a) variational evolution; (b) gradualism rather than large leaps; (c) processes of phyletic evolution and of speciation; (d) causes for the formation of varying individuals in populations and for the action of selective agents; and (e) all organisms evolved from a common ancestor. The first four are nomological-deductive explanations and the fifth is historical-narrative. Therefore evolutionary theory must be divided into nomological and historical theories which are both testable against objective empirical observations. To be scientific, historical evolutionary theories must be based on well corroborated nomological theories, both evolutionary and functional. Nomological and general historical evolutionary theories are well tested and must be considered as strongly corroborated scientific theories. Opponents of evolutionary theory are concerned only with historical evolutionary theories, having little interest in nomological theory. Yet given a well corroborated nomological evolutionary theory, historical evolutionary theories follow automatically. If understood correctly, both forms of evolutionary theories stand on their own as corroborated scientific theories and should not be labeled as facts.     

Advancing the metabolic theory of biodiversity

A component of metabolic scaling theory has worked towards understanding the influence of metabolism over the generation and maintenance of biodiversity. Specific models within this ‘metabolic theory of biodiversity’ (MTB) have addressed temperature gradients in speciation rate and species richness, but the scope of MTB has been questioned because of empirical departures from model predictions. In this study, we first show that a generalized MTB is not inconsistent with empirical patterns and subsequently implement an eco‐evolutionary MTB which has thus far only been discussed qualitatively. More specifically, we combine a functional trait (body mass) approach and an environmental gradient (temperature) with a dynamic eco‐evolutionary model that builds on the current MTB. Our approach uniquely accounts for feedbacks between ecological interactions (size‐dependent competition and predation) and evolutionary rates (speciation and extinction). We investigate a simple example in which temperature influences mutation rate, and show that this single effect leads to dynamic temperature gradients in macroevolutionary rates and community structure. Early in community evolution, temperature strongly influences speciation and both speciation and extinction strongly influence species richness. Through time, niche structure evolves, speciation and extinction rates fall, and species richness becomes increasingly independent of temperature. However, significant temperature‐richness gradients may persist within emergent functional (trophic) groups, especially when niche breadths are wide. Thus, there is a strong signal of both history and ecological interactions on patterns of species richness across temperature gradients. More generally, the successful implementation of an eco‐evolutionary MTB opens the perspective that a process‐based MTB can continue to emerge through further development of metabolic models that are explicit in terms of functional traits and environmental gradients.     

Effects of neutrality and productivity on mammal richness and evolutionary history in Australia

Explaining how heterogeneous spatial patterns of species diversity emerge is one of the most fascinating questions of biogeography. One of the great challenges is revealing the mechanistic effect of environmental variables on diversity. Correlative analyses indicate that productivity is associated with taxonomic, phylogenetic, and functional diversity of communities. Surprisingly, no unifying body of theory have been developed to understand the mechanism by which spatial variation of productivity affects the fundamental processes of biodiversity. Based on widely discussed verbal models in ecology about the effect of productivity on species diversity, we developed a spatially explicit neutral model that incorporates the effect of primary productivity on community size and confronted our model's predictions with observed patterns of species richness and evolutionary history of Australian terrestrial mammals. The imposed restrictions on community size create larger populations in areas of high productivity, which increases community turnover and local speciation, and reduces extinction. The effect of productivity on community size modeled in our study causes higher accumulation of species diversity in productive regions even in the absence of niche‐based processes. However, such a simple model is not capable of reproducing spatial patterns of mammal evolutionary history in Australia, implying that more complex evolutionary mechanisms are involved. Our study demonstrates that the overall patterns of species richness can be directly explained by changes in community sizes along productivity gradients, supporting a major role of processes associated with energetic constraints in shaping diversity patterns.     

WHAT WE HAVE ALSO LEARNED: ADAPTIVE SPECTIATION IS THEORETICALLY PLAUSIBLE

Abstract A recent Perspectives article by Gavrilets (2003) on the theory of speciation ignored advances in understanding processes of adaptive speciation, in which the splitting of lineages is an adaptation caused by frequency‐dependent selection. Adaptive, or sympatric, speciation has been modeled since the 1960s, but the large amount of attention from both empirical and theoretical biologists that adaptive speciation has received in recent years goes far beyond what was described in Gavrilets' paper. Due to conceptual advances based on the theory of adaptive dynamics, adaptive speciation has emergedj as a theoretically plausible evolutionary process that can occur in many different ecological settings.     

A generalized model of island biogeography

MacArthur and Wilson’s equilibrium theory is one of the most influential theories in ecology. Although evolution on islands is to be important to island biodiversity, speciation has not been well integrated into island biogeography models. By incorporating speciation and factors influencing it into the MacArthur-Wilson model, we propose a generalized model unifying ecological and evolutionary processes and island features. Intra-island speciation may play an important role in both island species richness and endemism, and the contribution of speciation to local species diversity may eventually be greater than that of immigration under certain conditions. Those conditions are related to the per species speciation rate, per species extinction rate, and island features, and they are independent of immigration rate. The model predicts that large islands will have a high, though not the highest, proportional endemism when other parameters are fixed. Based on the generalized model, changes in species richness and endemism on an oceanic island over time were predicted to be similar to empirical observations. Our model provides an ideal starting point for re-evaluating the role of speciation and re-analyzing available data on island species diversity, especially those biased by the MacArthur-Wilson model.     

What we have also learned: adaptive speciation is theoretically plausible

A recent Perspectives article by Gavrilets (2003) on the theory of speciation ignored advances in understanding processes of adaptive speciation, in which the splitting of lineages is an adaptation caused by frequency-dependent selection. Adaptive, or sympatric, speciation has been modeled since the 1960s, but the large amount of attention from both empirical and theoretical biologists that adaptive speciation has received in recent years goes far beyond what was described in Gavrilets' paper. Due to conceptual advances based on the theory of adaptive dynamics, adaptive speciation has emerged as a theoretically plausible evolutionary process that can occur in many different ecological settings.     

Genomic consequences of multiple speciation processes in a stick insect

Diverse geographical modes and mechanisms of speciation are known, and individual speciation genes have now been identified. Despite this progress, genome-wide outcomes of different evolutionary processes during speciation are less understood. Here, we integrate ecological and spatial information, mating trials, transplantation data and analysis of 86 130 single nucleotide polymorphisms (SNPs) in eight populations (28 pairwise comparisons) of Timema cristinae stick insects to test the effects of different factors on genomic divergence in a system undergoing ecological speciation. We find patterns consistent with effects of numerous factors, including geographical distance, gene flow, divergence in host plant use and climate, and selection against maladaptive hybridization (i.e. reinforcement). For example, the number of highly differentiated ‘outlier loci’, allele-frequency clines and the overall distribution of genomic differentiation were recognizably affected by these factors. Although host use has strong effects on phenotypic divergence and reproductive isolation, its effects on genomic divergence were subtler and other factors had pronounced effects. The results demonstrate how genomic data can provide new insights into speciation and how genomic divergence can be complex, yet predictable. Future work could adopt experimental, mapping and functional approaches to directly test which genetic regions are affected by selection and determine their physical location in the genome.     

Which evolutionary processes influence natural genetic variation for phenotypic traits?

Although many studies provide examples of evolutionary processes such as adaptive evolution, balancing selection, deleterious variation and genetic drift, the relative importance of these selective and stochastic processes for phenotypic variation within and among populations is unclear. Theoretical and empirical studies from humans as well as natural animal and plant populations have made progress in examining the role of these evolutionary forces within species. Tentative generalizations about evolutionary processes across species are beginning to emerge, as well as contrasting patterns that characterize different groups of organisms. Furthermore, recent technical advances now allow the combination of ecological measurements of selection in natural environments with population genetic analysis of cloned QTLs, promising advances in identifying the evolutionary processes that influence natural genetic variation.     

Making inferences about speciation using sophisticated statistical genetics methods: look before you leap

Understanding speciation is a fundamental aim of evolutionary biology and a very challenging one. Speciation can be viewed as the dynamics of genetic differentiation between populations resulting in substantial reproductive isolation (Gavrilets 2003). It was generally accepted that very small levels of migration prevent genetic differentiation among populations and, therefore, speciation. However, recent theoretical work showed that sympatric speciation is possible (Gavrilets 2003). Nevertheless, providing empirical evidence that gene flow occurred during speciation is challenging because several gene flow scenarios can explain observed patterns of genetic differentiation. Positive migration rate estimates alone do not prove ongoing gene flow during divergence. We also need to know whether migration took place before, during or after speciation. There is no statistical method specifically aimed at estimating gene flow timing, but several studies used the isolation with migration model (Hey & Nielsen 2004, 2007; Hey 2010b) to estimate this parameter and make inferences about speciation scenarios. It is tempting to use statistical methods to estimate important evolutionary parameters even if they do not appear explicitly in the inference model. Nevertheless, before doing so, we need to determine whether they can provide reliable results. In this issue of Molecular Ecology, Strasburg and Rieseberg (2011) present a simulation study that examines the degree to which gene flow timing estimates obtained from IMa2 (Hey 2010b) can be used to make inferences about speciation mode. Their results are sobering; gene flow timing estimates obtained in this way are not reliable and cannot be used to unequivocally establish if gene flow was ongoing during speciation.     

ISLAND BIOGEOGRAPHY AND PALAEOBIOLOGY: IN SEARCH FOR EVOLUTIONARY EQUILIBRIA

1. The concept of evolutionary equilibrium has been derived from the theory of island biogeography via an ecological rationale for increase in species extinction rate and decrease in speciation rate with increasing diversity of the system.
2. This concept is theoretically plausible at the species level and at a regional scale but, in spite of several empirical tests in the fossil record, it has thus far remained unsupported by empirical evidence. In order to test it conclusively, one has to analyze not only the pattern of species number through time but also its relationship to speciation and species extinction rates; independent evidence for perturbations must also be available.
3. The concept of evolutionary equilibrium at the global scale must be extrapolated over higher levels of taxonomic hierarchy, for reliable species-level data are unavailable at this scale. A theoretical justification for this concept cannot, then, be derived from the theory of island biogeography.
4. The rates of family extinction and origination in the Phanerozoic show no evidence for diversity-dependence, which undermines most quantitative models of biotic diversification based on the concept of global evolutionary equilibrium. Rigorous testing of these models cannot be done at the present state of knowledge because of the uncertainty about the empirical pattern (sampling and taxonomic biases, absolute time scale).     

Modes of speciation and the neutral theory of biodiversity

Hubbell's neutral theory of biodiversity has generated much debate over the need for niches to explain biodiversity patterns. Discussion of the theory has focused on its neutrality assumption, i.e. the functional equivalence of species in competition and dispersal. Almost no attention has been paid to another critical aspect of the theory, the assumptions on the nature of the speciation process. In the standard version of the neutral theory each individual has a fixed probability to speciate. Hence, the speciation rate of a species is directly proportional to its abundance in the metacommunity. We argue that this assumption is not realistic for most speciation modes because speciation is an emergent property of complex processes at larger spatial and temporal scales and, consequently, speciation rate can either increase or decrease with abundance. Accordingly, the assumption that speciation rate is independent of abundance (each species has a fixed probability to speciate) is a more natural starting point in a neutral theory of biodiversity. Here we present a neutral model based on this assumption and we confront this new model to 20 large data sets of tree communities, expecting the new model to fit the data better than Hubbell's original model. We find, however, that the data sets are much better fitted by Hubbell's original model. This implies that species abundance data can discriminate between different modes of speciation, or, stated otherwise, that the mode of speciation has a large impact on the species abundance distribution. Our model analysis points out new ways to study how biodiversity patterns are shaped by the interplay between evolutionary processes (speciation, extinction) and ecological processes (competition, dispersal).     

ON THE INDEPENDENCE OF SYSTEMATICS

Abstract— Before the publication of On the Origin of Species the standing patterns of natural history—common plan, homology, ontogenetic parallelism, and the hierarchy of groups — were taken as indications of a biological order that had not yet been understood. Darwin covered all of these in chapter 13 of the Origin , arguing that his theory was the first to provide a reasonable explanation for the existence of such patterns. Since Darwin took these relations to be established by previous biology, and used them as evidence for the explanatory power of his theory, he was clearly of the opinion that they were independent of that theory. Although several modern figures have argued to the contrary, it seems that Darwin was right. The patterns listed above are recoverable from observation without reference to evolutionary theory, which theory may then be applied to provide an account of the processes by which they may have come about. That aspect of systematics concerned with the identification of the empirical patterns evidently constitutes a study prior to and independent of theories of process.     

What is speciation and how should we study it?

To understand speciation, we first need to know what species are. Yet debates over species concepts have seemed endless, with little obvious relevance to the study of speciation. Recently, there has been progress in resolving these debates, favoring a lineage-based, evolutionary species concept. This progress calls for reconsideration of the study of speciation. Traditional speciation research based on the biological species concept has led to great advances in understanding how nonallopatric speciation occurs and how species diverge and remain separate from each other. However, this research has neglected the question of how new species arise in the first place for the most common geographic mode (allopatric). A new and very different research program is needed to understand the ecological and evolutionary processes that split an ancestral species into new allopatric lineages. This research program will connect speciation to many other fundamental questions in evolutionary biology, ecology, biogeography, and conservation biology.     

Using theoretical models to explore dispersal variation and fragmentation in urban environments

Cities are fundamentally changing the environment that plants inhabit, most notably through habitat fragmentation. Urban plant habitat patches are separated by impervious surfaces like buildings and roads and may vary from small, isolated green spaces to large green spaces like parks. Understanding the consequences of this urban fragmentation on seed dispersal is essential to both maintain urban biodiversity and mitigate the spread of unwanted weeds or invasive species but we currently lack enough empirical data to draw generalities. Theoretical reasoning (via both verbal and mathematical models) is well positioned to contribute to this knowledge gap in dispersal by providing useful predictions when empirical data are lacking. Variation in dispersal can easily be captured by models by incorporating different dispersal kernel shapes, and multiple habitat configurations can be examined. Urban environments are rarely considered by mathematical models, and our literature review indicates that most models that include dispersal variation via a dispersal kernel use only one or two shapes, suggesting a gap in the theoretical literature as well. We present a proof-of-concept model of fragmentation in an urban environment illustrating how varying habitat width can lead to different outcomes depending on the dispersal kernel. We also provide some thoughts for future directions on the application of mathematical models in urban areas.     

基于生物学物种定义探讨物种形成理论与验证的研究进展

物种形成是进化生物学研究的一个永恒主题, 由于生物群体进化是连续和动态的, 物种界限变得难于界定。本文首先讨论了3种地理物种形成模式(同域、邻域及异域), 并分析了近期报道的研究证据。其次, 评述了合子后生殖隔离机制的分子遗传基础和应用群体基因组数据分析的证据, 包括BDMI模型(Bateson-Dobzhansky-Muller incompatibility)、QTLs (quantitative trait loci)、霍尔丹法则及大X染色体效应。最后, 探讨了交配系统作为合子前隔离机制之一与物种形成的关系, 认为近交或自交通过扩大种群遗传结构分化, 增强不同交配系统的种群间不对称基因渐渗, 或种群间无基因渐渗等途径, 促进新物种形成。已知植物交配系统的演化更倾向于从异交(或自交不亲和)向自交(或近交亲和)方式, 花性状和基因组的分化推动形成所谓的自交综合征, 研究交配系统驱动或强化物种形成模式对认识植物物种形成机制有重要意义。     

Synergistic selection between ecological niche and mate preference primes diversification

The ecological niche and mate preferences have independently been shown to be important for the process of speciation. Here, we articulate a novel mechanism by which ecological niche use and mate preference can be linked to promote speciation. The degree to which individual niches are narrow and clustered affects the strength of divergent natural selection and population splitting. Similarly, the degree to which individual mate preferences are narrow and clustered affects the strength of divergent sexual selection and assortative mating between diverging forms. This novel perspective is inspired by the literature on ecological niches; it also explores mate preferences and how they may contribute to speciation. Unlike much comparative work, we do not search for evolutionary patterns using proxies for adaptation and sexual selection, but rather we elucidate how ideas from niche theory relate to mate preference, and how this relationship can foster speciation. Recognizing that individual and population niches are conceptually and ecologically linked to individual and population mate preference functions will significantly increase our understanding of rapid evolutionary diversification in nature. It has potential to help solve the difficult challenge of testing the role of sexual selection in the speciation process. We also identify ecological factors that are likely to affect individual niche and individual mate preference in synergistic ways and as a consequence to promote speciation. The ecological niche an individual occupies can directly affect its mate preference. Clusters of individuals with narrow, differentiated niches are likely to have narrow, differentiated mate preference functions. Our approach integrates ecological and sexual selection research to further our understanding of diversification processes. Such integration may be necessary for progress because these processes seem inextricably linked in the natural world.     

Speciation by natural and sexual selection: models and experiments

A large number of mathematical models have been developed that show how natural and sexual selection can cause prezygotic isolation to evolve. This article attempts to unify this literature by identifying five major elements that determine the outcome of speciation caused by selection: a form of disruptive selection, a form of isolating mechanism (assortment or a mating preference), a way to transmit the force of disruptive selection to the isolating mechanism (direct selection or indirect selection), a genetic basis for increased isolation (a one- or two-allele mechanism), and an initial condition (high or low initial divergence). We show that the geographical context of speciation (allopatry vs. sympatry) can be viewed as a form of assortative mating. These five elements appear to operate largely independently of each other and can be used to make generalizations about when speciation is most likely to happen. This provides a framework for interpreting results from laboratory experiments, which are found to agree generally with theoretical predictions about conditions that are favorable to the evolution of prezygotic isolation.     

On the theoretical and empirical framework for studying genetic interactions within and among species

We present a quantitative genetic (QG) interpretation of the Bateson-Dobzhansky-Muller (BDM) genetic model of speciation in order to unify the theoretical framework for understanding how the genetic differentiation of populations is associated with the process of speciation. Specifically, we compare the QG theory of joint scaling with the Turelli-Orr mathematical formulation of the BDM model. By formally linking the two models, we show that a wealth of empirical methods from QG can be brought to bear on the study of the genetic architecture of hybrid phenotypes to better understand the connections, if any, between microevolution within populations and macroevolution in the origin of species. By integrating the two theories, we make additional novel predictions that enrich the opportunities for empirically testing speciation genetic theory or facets of it, such as Haldane's rule. We show that the connection between the two theories is simple and straightforward for autosomal genes but not for sex-linked genes. Differences between the two approaches highlight key conceptual issues concerning the relevance of epistasis to evolution within and among lineages and to differences in the process of speciation in hermaphrodites and in organisms with separate sexes.     

Satellite species in lampreys: a worldwide trend for ecological speciation in sympatry?

Amongst several theories of speciation, sympatric speciation has been the most controversial but it is now widely accepted that populations can become reproductively isolated without being separated geographically. One problem with the acceptance of the theory of sympatric speciation, however, has been the lack of supporting empirical data and it is still believed that geographical isolation is responsible for the majority of speciation events. Here the example of species pairs in lampreys suggests that sympatric speciation in a whole taxonomic group could occur throughout its worldwide range. Lampreys occur in two ecologically distinct forms: parasitic mostly anadromous species that forage on tissue and body fluids of host fishes, and non‐parasitic forms that, apart from a short adult life when they cease feeding, spend their entire life as filter feeders in the substratum of stream beds. Both forms occur in sympatric species pairs throughout the range of lampreys that occur in Eurasia, North America and Australia and it is widely acknowledged that non‐parasitic forms derive from parasitic forms. The larvae of both forms can be distinguished by their potential fecundity and therefore, it is argued that the mode of life is not a consequence of different ecological conditions. Furthermore, as lampreys prefer to choose mates of similar sizes and fertilization success decreases with increasing difference in body size, there is a strong disruptive selection between the two forms and they are therefore reproductively isolated. Besides theoretical aspects, the similarity of the species pairs, together with their occurrence in sympatry, the occurrence of forms with intermediate characteristics, and examples where speciation might be in progress, hints at the possibility that speciation also occurred in sympatry. The difference between lampreys and other examples of sympatric speciation is that there seems to be a trend towards sympatric speciation events throughout the worldwide range of lampreys which is neither restricted to relatively small localities nor caused by human disturbance. Species pairs in lampreys therefore offer a unique possibility of studying the process of sympatric speciation on a large scale.