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.     

Speciation and the neutral theory of biodiversity

The neutral theory of biodiversity purports that patterns in the distribution and abundance of species do not depend on adaptive differences between species (i.e. niche differentiation) but solely on random fluctuations in population size (“ecological drift”), along with dispersal and speciation. In this framework, the ultimate driver of biodiversity is speciation. However, the original neutral theory made strongly simplifying assumptions about the mechanisms of speciation, which has led to some clearly unrealistic predictions. In response, several recent studies have combined neutral community models with more elaborate speciation models. These efforts have alleviated some of the problems of the earlier approaches, while confirming the general ability of neutral theory to predict empirical patterns of biodiversity. However, the models also show that the mode of speciation can have a strong impact on relative species abundances. Future work should compare these results to diversity patterns arising from non‐neutral modes of speciation, such as adaptive radiations.     

African cichlid fish: a model system in adaptive radiation research

The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.     

Lizards as model organisms for linking phylogeographic and speciation studies

Lizards have been model organisms for ecological and evolutionary studies from individual to community levels at multiple spatial and temporal scales. Here we highlight lizards as models for phylogeographic studies, review the published population genetics/phylogeography literature to summarize general patterns and trends and describe some studies that have contributed to conceptual advances. Our review includes 426 references and 452 case studies: this literature reflects a general trend of exponential growth associated with the theoretical and empirical expansions of the discipline. We describe recent lizard studies that have contributed to advances in understanding of several aspects of phylogeography, emphasize some linkages between phylogeography and speciation and suggest ways to expand phylogeographic studies to test alternative pattern‐based modes of speciation. Allopatric speciation patterns can be tested by phylogeographic approaches if these are designed to discriminate among four alternatives based on the role of selection in driving divergence between populations, including: (i) passive divergence by genetic drift; (ii) adaptive divergence by natural selection (niche conservatism or ecological speciation); and (iii) socially‐mediated speciation. Here we propose an expanded approach to compare patterns of variation in phylogeographic data sets that, when coupled with morphological and environmental data, can be used to to discriminate among these alternative speciation patterns. [Correction made after online publication (28/07/2010): (minor deletion in the last line of the abstract)].     

Non-ecological speciation, niche conservatism and thermal adaptation: how are they connected?

During the last decade, the ecological theory of adaptive radiation, and its corollary ??ecological speciation??, has been a major research theme in evolutionary biology. Briefly, this theory states that speciation is mainly or largely the result of divergent selection, arising from niche differences between populations or incipient species. Reproductive isolation evolves either as a result of direct selection on mate preferences (e.g. reinforcement), or as a correlated response to divergent selection (??by-product speciation??). Although there are now many tentative examples of ecological speciation, I argue that ecology??s role in speciation might have been overemphasised and that non-ecological and non-adaptive alternatives should be considered more seriously. Specifically, populations and species of many organisms often show strong evidence of niche conservatism, yet are often highly reproductively isolated from each other. This challenges niche-based ecological speciation and reveals partial decoupling between ecology and reproductive isolation. Furthermore, reproductive isolation might often evolve in allopatry before ecological differentiation between taxa or possibly through learning and antagonistic sexual interactions, either in allopatry or sympatry. Here I discuss recent theoretical and empirical work in this area, with some emphasis on odonates (dragonflies and damselflies) and suggest some future avenues of research. A main message from this paper is that the ecology of species differences is not the same as ecological speciation, just like the genetics of species differences does not equate to the genetics of speciation.     

What do we need to know about speciation?

Speciation has been a major focus of evolutionary biology research in recent years, with many important advances. However, some of the traditional organising principles of the subject area no longer provide a satisfactory framework, such as the classification of speciation mechanisms by geographical context into allopatric, parapatric and sympatry classes. Therefore, we have asked where speciation research should be directed in the coming years. Here, we present a distillation of questions about the mechanisms of speciation, the genetic basis of speciation and the relationship between speciation and diversity. Our list of topics is not exhaustive; rather we aim to promote discussion on research priorities and on the common themes that underlie disparate speciation processes.     

The speciation view: Disentangling multiple causes of adaptive and non-adaptive radiation in terms of speciation

Biological diversification often includes burst of lineage splitting. Such “radiation” has been known to act as evolutionary arenas with the potential to generate unique phylogenetic clusters and further novel groups. Although these radiations when accompanied by ecological diversification, so-called “adaptive radiation” have persisted as a central premise in evolutionary biology, the ecological and genetic mechanism of such rapid diversification has remained unclear. There are several critical definitions for the pattern of adaptive radiation, and those provide delimitation of adaptive and non-adaptive radiation. That being said, only a few studies have provided any clear demarcations in our understanding of the adaptive and non-adaptive causes of radiation from the mechanism of speciation. Here, we review the current consensus for the causes of adaptive radiation, especially along with the recent theoretical synthesis of “ecological speciation.” Further, we suggest the signature of adaptive and non-adaptive radiation in the earliest stages of diversification from the viewpoint of speciation. These criteria from the speciation view are useful to find the cases with the signatures of adaptive/non-adaptive radiation.     

Sympatric speciation by sexual selection: a critical reevaluation

Several empirical studies put forward sexual selection as an important driving force of sympatric speciation. This idea agrees with recent models suggesting that speciation may proceed by means of divergent Fisherian runaway processes within a single population. Notwithstanding this, the models so far have not been able to demonstrate that sympatric speciation can unfold as a fully adaptive process driven by sexual selection alone. Implicitly or explicitly, most models rely on nonselective factors to initiate speciation. In fact, they do not provide a selective explanation for the considerable variation in female preferences required to trigger divergent runaway processes. We argue that such variation can arise by disruptive selection but only when selection on female preferences is frequency dependent. Adaptive speciation is therefore unattainable in traditional female choice models, which assume selection on female preferences to be frequency independent. However, when frequency-dependent sexual selection processes act alongside mate choice, truly adaptive sympatric speciation becomes feasible. Speciation is then initiated independently of nonadaptive processes and does not suffer from the theoretical weaknesses associated with the current Fisherian runaway model of speciation. However, adaptive speciation requires the simultaneous action of multiple mechanisms, and therefore it occurs under conditions far more restrictive than earlier models of sympatric speciation by sexual selection appear to suggest.     

Speciation in the apple maggot fly: a blend of vintages?

The importance of speciation without the complete geographical separation of diverging populations (sympatric speciation) has become increasingly accepted. One of the textbook examples of recent speciation in sympatry is the apple maggot fly Rhagoletis pomonella, in which genetically differentiated host races feed on either hawthorn or apple. Three recent articles by Feder and collaborators show that the history of these host races is more complicated than was previously realized. Genes that differentiate races of flies that feed on either apple or hawthorn are located in chromosomal rearrangements. This variation forms a latitudinal cline that must have been established long before apples were available as hosts. Furthermore, there is also new evidence for the very recent evolution of a derived preference for volatile chemicals that are typical of apple fruits among apple-feeding flies. These results show that adaptation to apple populations has involved both the sorting of ancestral adaptive variation and the selection of novel mutations.     

Hybridization and adaptive radiation

Whether interspecific hybridization is important as a mechanism that generates biological diversity is a matter of controversy. Whereas some authors focus on the potential of hybridization as a source of genetic variation, functional novelty and new species, others argue against any important role, because reduced fitness would typically render hybrids an evolutionary dead end. By drawing on recent developments in the genetics and ecology of hybridization and on principles of ecological speciation theory, I develop a concept that reconciles these views and adds a new twist to this debate. Because hybridization is common when populations invade new environments and potentially elevates rates of response to selection, it predisposes colonizing populations to rapid adaptive diversification under disruptive or divergent selection. I discuss predictions and suggest tests of this hybrid swarm theory of adaptive radiation and review published molecular phylogenies of adaptive radiations in light of the theory.     

Does Speciation between Arabidopsis halleri and Arabidopsis lyrata Coincide with Major Changes in a Molecular Target of Adaptation?

Ever since Darwin proposed natural selection as the driving force for the origin of species, the role of adaptive processes in speciation has remained controversial. In particular, a largely unsolved issue is whether key divergent ecological adaptations are associated with speciation events or evolve secondarily within sister species after the split. The plant Arabidopsis halleri is one of the few species able to colonize soils highly enriched in zinc and cadmium. Recent advances in the molecular genetics of adaptation show that the physiology of this derived ecological trait involves copy number expansions of the AhHMA4 gene, for which orthologs are found in single copy in the closely related A. lyrata and the outgroup A. thaliana. To gain insight into the speciation process, we ask whether adaptive molecular changes at this candidate gene were contemporary with important stages of the speciation process. We first inferred the scenario and timescale of speciation by comparing patterns of variation across the genomic backgrounds of A. halleri and A. lyrata. Then, we estimated the timing of the first duplication of AhHMA4 in A. halleri. Our analysis suggests that the historical split between the two species closely coincides with major changes in this molecular target of adaptation in the A. halleri lineage. These results clearly indicate that these changes evolved in A. halleri well before industrial activities fostered the spread of Zn- and Cd-polluted areas, and suggest that adaptive processes related to heavy-metal homeostasis played a major role in the speciation process.     

Ecology and the origin of species

The ecological hypothesis of speciation is that reproductive isolation evolves ultimately as a consequence of divergent natural selection on traits between environments. Ecological speciation is general and might occur in allopatry or sympatry, involve many agents of natural selection, and result from a combination of adaptive processes. The main difficulty of the ecological hypothesis has been the scarcity of examples from nature, but several potential cases have recently emerged. I review the mechanisms that give rise to new species by divergent selection, compare ecological speciation with its alternatives, summarize recent tests in nature, and highlight areas requiring research.     

Theory and speciation

The study of speciation has become one of the most active areas of evolutionary biology, and substantial progress has been made in documenting and understanding phenomena ranging from sympatric speciation and reinforcement to the evolutionary genetics of postzygotic isolation. This progress has been driven largely by empirical results, and most useful theoretical work has concentrated on making sense of empirical patterns. Given the complexity of speciation, mathematical theory is subordinate to verbal theory and generalizations about data. Nevertheless, mathematical theory can provide a useful classification of verbal theories; can help determine the biological plausibility of verbal theories; can determine whether alternative mechanisms of speciation are consistent with empirical patterns; and can occasionally provide predictions that go beyond empirical generalizations. We discuss recent examples of progress in each of these areas.     

Searching for Sympatric Speciation in the Genomic Era

Sympatric speciation illustrates how natural and sexual selection may create new species in isolation without geographic barriers. However, recent genomic reanalyses of classic examples of sympatric speciation reveal complex histories of secondary gene flow from outgroups into the radiation. In contrast, the rich theoretical literature on this process distinguishes among a diverse range of models based on simple genetic histories and different types of reproductive isolating barriers. Thus, there is a need to revisit how to connect theoretical models of sympatric speciation and their predictions to empirical case studies in the face of widespread gene flow. Here, theoretical differences among different types of sympatric speciation and speciation‐with‐gene‐flow models are reviewed and summarized, and genomic analyses are proposed for distinguishing which models apply to case studies based on the timing and function of adaptive introgression. Investigating whether secondary gene flow contributed to reproductive isolation is necessary to test whether predictions of theory are ultimately borne out in nature.     

Evolution and speciation on holey adaptive landscapes

Sewall Wright's powerful metaphor of rugged adaptive landscapes has formed the basis for discussing evolution and speciation for more than 60 years. However, this metaphor, with its emphasis on adaptive peaks and valleys, is to a large degree a reflection of our three-dimensional experience. Both genotypes and phenotypes of biological organisms differ in numerous characteristics, and, thus, the dimension of 'real' adaptive landscapes is much larger than three. Properties of multidimensional adaptive landscapes are very different from those of low dimension. Consequently, something that is seen as a theoretical challenge in a low-dimensional case might be a trivial problem in a multidimensional context and vice versa. In particular, the problem of how a population crosses an adaptive valley on its way from one adaptive peak to another, which Wright attempted to solve with his shifting balance theory, may be non-existent. A new framework is emerging for deepening our understanding of evolution and speciation, which provides a plausible multidimensional alternative to the conventional view of rugged adaptive landscapes.     

CALIBRATING DIVERGENCE TIMES ON SPECIES TREES VERSUS GENE TREES: IMPLICATIONS FOR SPECIATION HISTORY OF APHELOCOMA JAYS

Estimates of the timing of divergence are central to testing the underlying causes of speciation. Relaxed molecular clocks and fossil calibration have improved these estimates; however, these advances are implemented in the context of gene trees, which can overestimate divergence times. Here we couple recent innovations for dating speciation events with the analytical power of species trees, where multilocus data are considered in a coalescent context. Divergence times are estimated in the bird genus Aphelocoma to test whether speciation in these jays coincided with mountain uplift or glacial cycles. Gene trees and species trees show general agreement that diversification began in the Miocene amid mountain uplift. However, dates from the multilocus species tree are more recent, occurring predominately in the Pleistocene, consistent with theory that divergence times can be significantly overestimated with gene‐tree based approaches that do not correct for genetic divergence that predates speciation. In addition to coalescent stochasticity, Haldane's rule could account for some differences in timing estimates between mitochondrial DNA and nuclear genes. By incorporating a fossil calibration applied to the species tree, in addition to the process of gene lineage coalescence, the present approach provides a more biologically realistic framework for dating speciation events, and hence for testing the links between diversification and specific biogeographic and geologic events.     

Ecology and speciation

Recent studies on diverse taxa suggest that natural selection caused by shifts in ecology or invasions of novel habitats plays an important role in adaptive divergence and speciation. Exciting new studies integrating approaches from both the field and the laboratory suggest that ecological shifts can result in extremely rapid rates of evolutionary divergence. Although experimental approaches that link rapid ecological divergence to reproductive isolation and speciation are in their infancy, recent research indicates those approaches that will be most useful.     

Schistosomes: the road from host-parasite interactions to vaccines in clinical trials

Insights over recent years into the interactions between helminths, including schistosomes, and the immune system have generated new concepts in immunology and significant advances in vaccine strategies. Here, we report recent advances that substantially increase our understanding of the nature of the host innate and adaptive responses to schistosomes and on strategies elaborated by the parasite to manipulate such responses. We also describe the long road that has allowed us to move from the identification of an anti-schistosome vaccine candidate, a 28kDa glutathione-S-transferase, to its recent evaluation in human clinical trials.     

Punctuated equilibrium in a neontological context

The theory of punctuated equilibrium, which proposes that biological species evolve rapidly when they originate rather than gradually over time, has sparked intense debate between palaeontologists and evolutionary biologists about the mode of character evolution and the importance of natural selection. Difficulty in interpreting the fossil record prevented consensus, and it remains disputed as to what extent gradual change in established species is responsible for phenotypic differences between species. Against the historical background of the concept of evolution concentrated in speciation events, we review attempts to investigate tempo and mode of evolution using present-day species since the introduction of the theory of punctuated equilibrium in 1972. We discuss advantages, disadvantages, and prospects of using neontological data, methodological advances, and the findings of some recent studies.