Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds

Although evolutionary theory predicts an association between the evolution of elaborate ornamentation and speciation, empirical evidence for links between speciation and ornament evolution has been mixed. In birds, the evolution of increasingly complex and colorful plumage may promote speciation by introducing prezygotic mating barriers. However, overall changes in color complexity, including both increases and decreases, may also promote speciation by altering the sexual signals that mediate reproductive choices. Here, we examine the relationship between complex plumage and speciation rates in the largest family of songbirds, the tanagers (Thraupidae). First, we test whether species with more complex plumage coloration are associated with higher speciation rates and find no correlation. We then test whether rates of male or female plumage color complexity evolution are correlated with speciation rates. We find that elevated rates of plumage complexity evolution are associated with higher speciation rates, regardless of sex and whether species are evolving more complex or less complex ornamentation. These results extend to whole-plumage color complexity and regions important in signaling (crown and throat) but not nonsignaling regions (back and wingtip). Our results suggest that the extent of change in plumage traits, rather than overall values of plumage complexity, may play a role in speciation.     

Reconstructing the evolution of birds on islands: 100 years of research

Birds, especially those on islands, have contributed disproportionately to the development of theories that explain the origin and maintenance of organic diversity. This essay surveys the major ideas of how bird species are thought to evolve, speciate and multiply in adaptive radiations on islands. I begin with the nineteenth century view that speciation is the result of natural selection slowly causing divergence of geographically separated populations. I then trace the course of discovery and deeper understanding during the twentieth century, from the influence of Mendelian genetics at the beginning to the modern, molecular era at the end. The dominant and pivotal evolutionary question has been how new species are formed. An initial, nearly exclusive, attention to adaptive processes has been replaced by a search for additional reasons for allopatric divergence, coupled with the conditions that permit coexistence in sympatry after allopatric divergence has occurred. Recent studies have shown that pre‐mating barriers to gene exchange caused by natural selection and sexual selection often arise before post‐mating genetic incompatibilities have evolved. Therefore behavioural and ecological factors play a predominant role in this stage of speciation. Imprinting and imprinting‐like processes of early learning contribute to pre‐mating barriers by constraining mate choice. Ecological factors determine coexistence potential and the fates of hybrids. Genetical factors at all stages, from the founding of a new population to the evolution of genetic incompatibilities, are still poorly known. But molecular genetics is now helping us to reconstruct evolutionary history, thereby transforming ideas about systematic relationships, colonization routes and both the tempo and mode of evolution. As patterns of evolution within radiations become better known, more attention needs to be given to the task of explaining the sequential build‐up of avian communities; by evolutionary radiation and additional immigration, offset to some extent by extinction. The new and substantial challenge is to understand evolutionary radiations in relation to changing environments. Until that challenge is met we cannot claim that the problem of explaining adaptive radiations of birds or any other group of organisms is solved.     

Ring species as bridges between microevolution and speciation

A demonstration of how small changes can lead to species-level differences is provided by ring species, in which two reproductively isolated forms are connected by a chain of intermediate populations. We review proposed cases of ring species and the insights they provide into speciation. Ring species have been viewed both as illustrations of the history of divergence of two species from their common ancestor and as demonstrations that speciation can occur in spite of gene flow between the diverging forms. Theoretical models predict that speciation with gene flow can occur when there is divergent ecological selection, and geographical differentiation increases the likelihood of speciation. Thus ring species are ideal systems for research into the role of both ecological and geographical differentiation in speciation, but few examples have been studied in detail. The Greenish warbler is a ring species in which two northward expansions around the Tibetan plateau have been accompanied by parallel evolution in morphology, ecology, and song length and complexity. However, songs have diverged in structure, resulting in a lack of recognition where the reproductively isolated forms come into contact in Siberia. Our analysis suggests that these differences could have arisen even with gene flow, and that parallel rather than divergent ecological changes have led to divergence in sexually selected traits and subsequent speciation.     

A metric for the study of evolutionary trends in the complexity of serial structures

Little empirical work has been done to see what sort of patterns of change in morphological complexity occur in evolution, mainly because the complexity of whole organisms has been so hard to define and to measure. For serial structures within organisms, there are fewer difficulties; this paper introduces a set of complexity metrics that are designed especially for serial structures, and then explores some of the properties of the new metrics. Also, a principle proposed in the last century by Herbert Spencer, and offered recently in a new form by the thermodynamic school of evolutionary thought, predicts that complexity should increase in evolution as a consequence of the accumulation of perturbations. Here, simulations in which perturbations are introduced to ideal and real series of vertebral measurements show how the complexity increase predicted by Spencer's principle would be captured by the new metrics.     

What are genes “for” or where are traits “from”? What is the question?

For at least a century it has been known that multiple factors play a role in the development of complex traits, and yet the notion that there are genes “for” such traits, which traces back to Mendel, is still widespread. In this paper, we illustrate how the Mendelian model has tacitly encouraged the idea that we can explain complexity by reducing it to enumerable genes. By this approach many genes associated with simple as well as complex traits have been identified. But the genetic architecture of biological traits, or how they are made, remains largely unknown. In essence, this reflects the tension between reductionism as the current “modus operandi” of science, and the emerging knowledge of the nature of complex traits. Recent interest in systems biology as a unifying approach indicates a reawakened acceptance of the complexity of complex traits, though the temptation is to replace “gene for” thinking by comparably reductionistic “network for” concepts. Both approaches implicitly mix concepts of variants and invariants in genetics. Even the basic question is unclear: what does one need to know to “understand” the genetic basis of complex traits? New operational ideas about how to deal with biological complexity are needed.     

Revisiting the particular role of host shifts in initiating insect speciation

The notion that shifts to new hosts can initiate insect speciation is more than 150 years old, yet widespread conflation with paradigms of sympatric speciation has led to confusion about how much support exists for this hypothesis. Here, we review 85 insect systems and evaluate the relationship between host shifting, reproductive isolation, and speciation. We sort insects into five categories: (1) systems in which a host shift has initiated speciation; (2) systems in which a host shift has made a contribution to speciation; (3) systems in which a host shift has caused the evolution of new reproductive isolating barriers; (4) systems with host‐associated genetic differences; and (5) systems with no evidence of host‐associated genetic differences. We find host‐associated genetic structure in 65 systems, 43 of which show that host shifts have resulted in the evolution of new reproductive barriers. Twenty‐six of the latter also support a role for host shifts in speciation, including eight studies that definitively support the hypothesis that a host shift has initiated speciation. While this review is agnostic as to the fraction of all insect speciation events to which host shifts have contributed, it clarifies that host shifts absolutely can and do initiate speciation.     

Do the constraints of human speciation cause expression of the same set of genes in brain, testis, and placenta?

Evolution appears to be especially rapid during speciation, and the genes involved in speciation should be evident in species such as humans that have recently speciated or are presently in the process of speciation. Haldane's rule is that when one sex is sterile or inviable in interspecific F(1) hybrids, it is usually the heterogametic sex. For mammals, this implicates genes on the X chromosome as those particularly responsible for speciation. A preponderance of sex- and reproduction-related genes on the X chromosome has been shown repeatedly, but also mental retardation genes are more frequent on the X chromosome. We argue that brain, testis, and placenta are those organs most responsible for human speciation. Furthermore, the high degree of complexity of the vertebrate genome demands coordinate evolution of new characters. This coordination is best attained when the same set of genes is redeployed for these new characters in the brain, testis, and placenta.     

The geography of mammalian speciation: mixed signals from phylogenies and range maps

The importance of geographic isolation in speciation has been debated since the 19th century. Since the beginning of the 20th century, the consensus has been that most speciation involves divergence in allopatry. This consensus was based largely on decades of observations by naturalists and verbal arguments against speciation without isolation. Recent attempts to quantify the importance of allopatric versus sympatric speciation using comparative methods called "age-range correlation" (ARC) suggest that allopatric speciation is more common than sympatric speciation. However, very few taxa have been studied and there are concerns about the adequacy of the methods. We propose methodological improvements including changes in the way overlap between clades is quantified and Monte Carlo methods to test the null hypothesis of no relationship between phylogenetic relatedness and geographic range overlap. We analyze 14 clades of mammals, chosen because of the availability of data and the consensus among mammalogists that speciation is routinely allopatric. Although data from a few clades clearly indicate allopatric speciation, divergence with gene flow is plausible in others and many results are inconclusive. The relative rarity of significant correlations between phylogenetic distance and range overlap may have three distinct causes: (1) post-speciation range changes, (2) relative rarity of range overlap, and (3) a mixture of geographic modes of speciation. Our results support skepticism about ARC's power for inferring the biogeography of speciation. Yet, even if few clades provide clear signals, meta-analytic approaches such as ARC may set bounds on the prevalence of alternative modes of speciation.     

Has the evolution of complexity in the amphibian papilla influenced anuran speciation rates?

For anurans, increasing complexity of the inner ear has been correlated with speciation rates. The evolution of a complex amphibian papilla (AP) is thought to have facilitated speciation by extending the range of frequencies over which mating calls may diverge. Although this example has been proposed to represent a key innovation, the mechanism by which the AP is thought to promote speciation makes the questionable assumption that anurans generally use the AP for detection of their mating calls. This study uses mating calls from 852 species to test this assumption. Surprisingly, the calls of most species are not detected by the AP but by a second organ, the basilar papilla (BP). This refutes the role of AP complexity in facilitating call divergence and hence, speciation. Future research into the evolution of acoustically mediated reproductive isolation should focus instead on the BP as it may play a more critical role in anuran speciation.     

Ecotypes and the controversy over stages in the formation of new species

Recent interest in the role of ecology in species formation has led to renewed discussion of the stages in the process of speciation. Although attempts to classify the stages in the process of species formation date back at least as far as Alfred Russel Wallace, one of the most intense debates on the subject occurred among botanists during the mid‐20th Century. The present review outlines the progression of the historical debate about stages in the evolution of species, which was instigated by the genecological classification scheme of Göte Turesson in the 1920s, championed in the mid‐century by Jens Clausen, and then brought under harsh scrutiny by many in the 1960s and 1970s. At the heart of the controversy is the question of whether speciation occurs rapidly on a local scale or gradually through the formation of geographically widespread ecotypes that evolve as precursors to species. A corollary to this debate is the question of whether speciation is reversible and, if so, how does it become irreversible? A third wave of interest in stages in the process of speciation is currently underway, thus making a modern historical narrative of the debate important. Both contemporary and past evolutionary biologists have argued that viewing speciation as being composed of stages can free researchers from concerns over species definitions and focus attention on the mechanisms involved in the process. How speciation becomes irreversible and whether ecogeographically isolated ecotypes are integral to this process remain as important unresolved issues. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 106 , 241–257.     

Performing Evolution: Role-Play Simulations

By simulating evolution through performance, students become physically, as well as mentally, engaged in thinking about evolutionary concepts. This instructional strategy redirects tension around the subject toward metacognitive reflection. Non-verbal performances like those presented here also avoid the pitfalls of relying on difficult-to-use language. This paper describes a teachable unit including the learning goals and outcomes as well as rubrics to aid assessment. Through two performance-based activities, the unit introduces the fundamental evolutionary concepts that evolution lacks forethought and that natural selection is a sorting process. By reflecting on the performances, students learn other sophisticated evolutionary concepts like hitchhiking, the effects of environmental change, and the extinction of traits. They also become aware of the scientific process, articulating hypotheses about the outcome of the simulations, collecting data, and revising their hypotheses. Discussions and homework about the performances reveal how learning progresses, and detailed rubrics help both instructors and students assess conceptual learning. This unit concludes with the opportunity for students to transfer what they have learned to new concepts: they design new performances to simulate other mechanisms of evolution, such as genetic drift, mutation, and migration.     

Speciation by symbiosis

In the Origin of Species, Darwin struggled with how continuous changes within a species lead to the emergence of discrete species. Molecular analyses have since identified nuclear genes and organelles that underpin speciation. In this review, we explore the microbiota as a third genetic component that spurs species formation. We first recall Ivan Wallin's original conception from the early 20th century on the role that bacteria play in speciation. We then describe three fundamental observations that justify a prominent role for microbes in eukaryotic speciation, consolidate exemplar studies of microbe-assisted speciation and incorporate the microbiota into classic models of speciation.     

When is sympatric speciation truly adaptive? An analysis of the joint evolution of resource utilization and assortative mating

The plausibility of sympatric speciation has long been debated among evolutionary ecologists. The process necessarily involves two key elements: the stable coexistence of at least two ecologically distinct types and the emergence of reproductive isolation. Recent theoretical studies within the theoretical framework of adaptive dynamics have shown how both these processes can be driven by natural selection. In the standard scenario, a population first evolves to an evolutionary branching point, next, disruptive selection promotes ecological diversification within the population, and, finally, the fitness disadvantage of intermediate types induces a selection pressure for assortative mating behaviour, which leads to reproductive isolation and full speciation. However, the full speciation process has been mostly studied through computer simulations and only analysed in part. Here I present a complete analysis of the whole speciation process by allowing for the simultaneous evolution of the branching ecological trait as well as a continuous trait controlling mating behaviour. I show how the joint evolution can be understood in terms of a gradient landscape, where the plausibility of different evolutionary paths can be evaluated graphically. I find sympatric speciation unlikely for scenarios with a continuous, unimodal, distribution of resources. Rather, ecological settings where the fitness inferiority of intermediate types is preserved during the ecological branching are more likely to provide opportunity for adaptive, sympatric speciation. Such scenarios include speciation due to predator avoidance or specialization on discrete resources. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Karyotypic evolution in Gehyra (Gekkonidae: Reptilia) IV. Chromosome change and speciation

Karyotypic data are presented for six additional species from the genus Gehyra collected in Australia, New Guinea and Fiji. C and G-banding of three of the very diverse species which all share the ancestral 2n=44 karyotype, further strengthens the phylogenetic model for the evolution of this complex. With 19 Australian species and chromosome races of Gehyra now karyotyped, it has been possible to evaluate the mode of chromosomal evolution and the role that chromosome change has played in speciation in this genus. It is clear that speciation in certain karyomorph groups has occurred allopatrically, without any gross chromosomal changes. However, in the numerous chromosome races and species which have been involved in colonizing radiations, chromosomal rearrangements have been intricately associated with the speciation process.     

The role of allochrony in speciation

The importance of sympatric speciation – the evolution of reproductive isolation between codistributed conspecific individuals – in generating biodiversity is highly controversial. Allochrony, or differences in breeding time (phenology) between conspecific individuals, has the potential to lead to reproductive isolation and therefore speciation. We critically review the literature to test the importance of allochronic speciation over the three timescales over which allochrony can occur – over the day, between seasons or between years – and explore what is known about genomic mechanisms underlying allochrony in the diverse taxa in which it is found. We found that allochrony can be a key contributor to reproductive isolation, especially if populations have little overlap in breeding time and therefore little potential for gene flow, and may sometimes be the initial or key driver of speciation. Shifts in phenology can be caused by several factors, including a new ecological opportunity, environmental change, or reinforcement. The underlying genomic basis of allochrony has been studied mostly in insects, highlighting the need for genomic studies in other taxa; nonetheless, results to date indicate that several cases of allochrony involve changes in circadian genes. This review provides the first comprehensive discussion of the role of allochrony in speciation and demonstrates that allochrony as a contributor to divergence may be more widespread than previously thought. Understanding genomic changes and adaptations allowing organisms to breed at new times may be key in the light of phenological changes required under climate change.     

MODELING PHENOTYPIC PLASTICITY IN GROWTH TRAJECTORIES: A STATISTICAL FRAMEWORK

Phenotypic plasticity, that is multiple phenotypes produced by a single genotype in response to environmental change, has been thought to play an important role in evolution and speciation. Historically, knowledge about phenotypic plasticity has resulted from the analysis of static traits measured at a single time point. New insight into the adaptive nature of plasticity can be gained by an understanding of how organisms alter their developmental processes in a range of environments. Recent advances in statistical modeling of functional data and developmental genetics allow us to construct a dynamic framework of plastic response in developmental form and pattern. Under this framework, development, genetics, and evolution can be synthesized through statistical bridges to better address how evolution results from phenotypic variation in the process of development via genetic alterations.     

Chromosomal rearrangements,genome reorganization,and speciation

Historical analysis of studying chromosome changes in evolution allows better understanding of the current level of research in this area. Reorganizations of the genetic system due to chromosomal rearrangements have important evolutionary consequences and may lead to speciation. Despite the complexity of evaluating the primacy of chromosome changes in speciation events, such phenomena are possible and occur in nature, as recent studies have demonstrated.     

Evolution of reproductive isolation in stickleback fish

To understand how new species form and what causes their collapse, we examined how reproductive isolation evolves during the speciation process, considering species pairs with little to extensive divergence, including a recently collapsed pair. We estimated many reproductive barriers in each of five sets of stickleback fish species pairs using our own data and decades of previous work. We found that the types of barriers important early in the speciation process differ from those important late. Two premating barriers—habitat and sexual isolation—evolve early in divergence and remain two of the strongest barriers throughout speciation. Premating isolation evolves before postmating isolation, and extrinsic isolation is far stronger than intrinsic. Completing speciation, however, may require postmating intrinsic incompatibilities. Reverse speciation in one species pair was characterized by significant loss of sexual isolation. We present estimates of barrier strengths before and after collapse of a species pair; such detail regarding the loss of isolation has never before been documented. Additionally, despite significant asymmetries in individual barriers, which can limit speciation, total isolation was essentially symmetric between species. Our study provides important insight into the order of barrier evolution and the relative importance of isolating barriers during speciation and tests fundamental predictions of ecological speciation.     

DRIFT PROMOTES SPECIATION BY SEXUAL SELECTION

Quantitative genetic models of sexual selection have generally failed to provide a direct connection to speciation and to explore the consequences of finite population size. The connection to speciation has been indirect because the models have treated only the evolution of male and female traits and have stopped short of modeling the evolution of sexual isolation. In this article we extend Lande's (1981) model of sexual selection to quantify predictions about the evolution of sexual isolation and speciation. Our results, based on computer simulations, support and extend Lande's claim that drift along a line of equilibria can rapidly lead to sexual isolation and speciation. Furthermore, we show that rapid speciation can occur by drift in populations of appreciable size ( N_e ≥ 1000). These results are in sharp contrast to the opinion of many researchers and textbook writers who have argued that drift does not play an important role in speciation. We argue that drift may be a powerful amplifier of speciation under a wide variety of modeling assumptions, even when selection acts directly on female mating preferences.