So what is a species anyway? A primatological perspective

Since Darwin's time, the question “what a species” has provoked fierce disputes and a tremendous number of publications, from short opinion papers to thick volumes. 1 The debates covered fundamental philosophical questions, such as: Do species exist at all independently of a human observer or are they just a construct of the human mind to categorize nature's organismic diversity and serve as a semantic tool in human communication about biodiversity? 2 - 4 or: Are species natural kinds (classes) or individuals that are “born” by speciation, change in course of time, and finally “die” when they go extinct or diverge into new species? 5 - 8 Also included was the problem of species as taxa (taxonomic) versus species as products of the speciation process (evolutionary). 9 More pragmatic issues arose, such as: How can we reliably delineate and delimitate species? 10 , 11 The great interest in what a species is reflects the importance of “species” as fundamental units in most fields of biology, especially evolutionary biology, ecology, and conservation. 2 , 12 - 14     

Cell death: questions for histochemists concerning the causes of the various cytological changes

Summary The question of cell death is accessible to study by histochemists and many questions remain to be resolved. From a physiological point of view, the most important are the causal relationships. (1) At what phase in cell death is the synthesis of RNA disrupted and at what phase is the rate of degradation of RNA increased? (2) Does the disruption of synthesis result from a direct genetic command, or does it result indirectly from gradual deterioration of energy resources or optimal ionic conditions? (3) What properties, presumably of the substrate organelles, marks them for specific absorption into autophagic vacuoles? (4) What proteases and other hydrolases operate currently undetected in the cytoplasm? How are they controlled and regulated? (5) Why does the physiologically dying cell shrink and appear more dense? To what extent is a cell in this state able to regulate any metabolic parameter? The advent of newer, more sensitive and quantitative techniques, and greater attention to the controls and causes as opposed to the phenomena, should help to resolve these questions.     

Five statistical questions about the tree of life

Stochastic modeling of phylogenies raises five questions that have received varying levels of attention from quantitatively inclined biologists. 1) How large do we expect (from the model) the ratio of maximum historical diversity to current diversity to be? 2) From a correct phylogeny of the extant species of a clade, what can we deduce about past speciation and extinction rates? 3) What proportion of extant species are in fact descendants of still-extant ancestral species, and how does this compare with predictions of models? 4) When one moves from trees on species to trees on sets of species (whether traditional higher order taxa or clades within PhyloCode), does one expect trees to become more unbalanced as a purely logical consequence of tree structure, without signifying any real biological phenomenon? 5) How do we expect that fluctuation rates for counts of higher order taxa should compare with fluctuation rates for number of species? We present a mathematician's view based on an oversimplified modeling framework in which all these questions can be studied coherently.     

Speciation across the Tree of Life

Much of what we know about speciation comes from detailed studies of well-known model systems. Although there have been several important syntheses on speciation, few (if any) have explicitly compared speciation among major groups across the Tree of Life. Here, we synthesize and compare what is known about key aspects of speciation across taxa, including bacteria, protists, fungi, plants, and major animal groups. We focus on three main questions. Is allopatric speciation predominant across groups? How common is ecological divergence of sister species (a requirement for ecological speciation), and on what niche axes do species diverge in each group? What are the reproductive isolating barriers in each group? Our review suggests the following patterns. (i) Based on our survey and projected species numbers, the most frequent speciation process across the Tree of Life may be co-speciation between endosymbiotic bacteria and their insect hosts. (ii) Allopatric speciation appears to be present in all major groups, and may be the most common mode in both animals and plants, based on non-overlapping ranges of sister species. (iii) Full sympatry of sister species is also widespread, and may be more common in fungi than allopatry. (iv) Full sympatry of sister species is more common in some marine animals than in terrestrial and freshwater ones. (v) Ecological divergence of sister species is widespread in all groups, including ~70% of surveyed species pairs of plants and insects. (vi) Major axes of ecological divergence involve species interactions (e.g. host-switching) and habitat divergence. (vii) Prezygotic isolation appears to be generally more widespread and important than postzygotic isolation. (viii) Rates of diversification (and presumably speciation) are strikingly different across groups, with the fastest rates in plants, and successively slower rates in animals, fungi, and protists, with the slowest rates in prokaryotes. Overall, our study represents an initial step towards understanding general patterns in speciation across all organisms.     

Speciation pathway of Isoetes (Isoetaceae) in East Asia inferred from molecular phylogenetic relationships

Polyploidy plays an important role in the speciation of Iso?tes. Increasing our knowledge about the specific origin of each polyploid or phylogenetic relationship among species has been hampered because of conserved morphological variation and scarce habitats. We present several hypotheses concerning the speciation pathways of Iso?tes species distributed in East Asia. Our hypotheses are inferred from phylogenetic relationships that were elucidated using sequences of the internal transcribed spacer regions of nuclear ribosomal DNA, a second intron of LEAFY, and chloroplast DNA trnS-psbC spacer regions. These inferred phylogenetic relationships indicated that (1) the Chinese tetraploid, I. sinensis, is closely related to I. yunguiensis; (2) the Korean endemic species, I. hallasanensis, is an autotetraploid derived from I. taiwanensis or closely related taxa; (3) the hexaploid I. coreana forms a clade and has its closest evolutionary relationships with I. taiwanensis or I. hallasanensis; and (4) the Japanese hexaploid I. japonica is closely related to I. taiwanensis-I. coreana and I. sinensis-I. yunguiensis. These results suggest that interspecific hybridization and polyploidization have played central roles in speciation of East Asian Iso?tes. Furthermore, I. taiwanensis, an endemic species in Taiwan, has been involved in at least three cases of autopolyploid or allopolyploid speciation in East Asia.     

Large-scale patterns in morphological diversity and species assemblages in Neotropical Triatominae (Heteroptera: Reduviidae)

We analysed the spatial variation in morphological diversity (MDiv) and species richness (SR) for 91 species of Neotropical Triatominae to determine the ecological relationships between SR and MDiv and to explore the roles that climate, productivity, environmental heterogeneity and the presence of biomes and rivers may play in the structuring of species assemblages. For each 110 km x 110 km-cell on a grid map of America, we determined the number of species (SR) and estimated the mean Gower index (MDiv) based on 12 morphological attributes. We performed bootstrapping analyses of species assemblages to identify whether those assemblages were more similar or dissimilar in their morphology than expected by chance. We applied a multi-model selection procedure and spatial explicit analyses to account for the association of diversity-environment relationships. MDiv and SR both showed a latitudinal gradient, although each peaked at different locations and were thus not strictly spatially congruent. SR decreased with temperature variability and MDiv increased with mean temperature, suggesting a predominant role for ambient energy in determining Triatominae diversity. Species that were more similar than expected by chance co-occurred near the limits of the Triatominae distribution in association with changes in environmental variables. Environmental filtering may underlie the structuring of species assemblages near their distributional limits.     

A framework for comparing processes of speciation in the presence of gene flow

How common is speciation‐with‐gene‐flow? How much does gene flow impact on speciation? To answer questions like these requires understanding of the common obstacles to evolving reproductive isolation in the face of gene flow and the factors that favour this crucial step. We provide a common framework for the ways in which gene flow opposes speciation and the potential conditions that may ease divergence. This framework is centred on the challenge shared by most scenarios of speciation‐with‐gene‐flow, i.e. the need for coupling among different components of reproductive isolation. Using this structure, we review and compare the factors favouring speciation with the intention of providing a more integrated picture of speciation‐with‐gene‐flow.     

THE BIOLOGY OF SPECIATION

Since Darwin published the “Origin,” great progress has been made in our understanding of speciation mechanisms. The early investigations by Mayr and Dobzhansky linked Darwin's view of speciation by adaptive divergence to the evolution of reproductive isolation, and thus provided a framework for studying the origin of species. However, major controversies and questions remain, including: When is speciation nonecological? Under what conditions does geographic isolation constitute a reproductive isolating barrier? and How do we estimate the “importance” of different isolating barriers? Here, we address these questions, providing historical background and offering some new perspectives. A topic of great recent interest is the role of ecology in speciation. “Ecological speciation” is defined as the case in which divergent selection leads to reproductive isolation, with speciation under uniform selection, polyploid speciation, and speciation by genetic drift defined as “nonecological.” We review these proposed cases of nonecological speciation and conclude that speciation by uniform selection and polyploidy normally involve ecological processes. Furthermore, because selection can impart reproductive isolation both directly through traits under selection and indirectly through pleiotropy and linkage, it is much more effective in producing isolation than genetic drift. We thus argue that natural selection is a ubiquitous part of speciation, and given the many ways in which stochastic and deterministic factors may interact during divergence, we question whether the ecological speciation concept is useful. We also suggest that geographic isolation caused by adaptation to different habitats plays a major, and largely neglected, role in speciation. We thus provide a framework for incorporating geographic isolation into the biological species concept (BSC) by separating ecological from historical processes that govern species distributions, allowing for an estimate of geographic isolation based upon genetic differences between taxa. Finally, we suggest that the individual and relative contributions of all potential barriers be estimated for species pairs that have recently achieved species status under the criteria of the BSC. Only in this way will it be possible to distinguish those barriers that have actually contributed to speciation from those that have accumulated after speciation is complete. We conclude that ecological adaptation is the major driver of reproductive isolation, and that the term “biology of speciation,” as proposed by Mayr, remains an accurate and useful characterization of the diversity of speciation mechanisms.     

Physiology and biophysics of chloride and cation cotransport across cell membranes

Many important questions remain to be answered about the mechanism that mediates coupled Na,K,Cl cotransport. We still do not know what the ATP requirement involves. Is ATP the direct energy source? Such an energy source does not seem to be necessary, inasmuch as the net free energy in the combined transmembrane chemical gradients of Na, K, and Cl is quite sufficient to maintain the observed high Cl(i). Could a protein kinase-mediated mechanism be responsible for the ATP requirement? How does reducing Cl(i) stimulate the transporter? What are the kinetic relationships for the co-ions at the outward- and inward-facing transport sites? Are they symmetrical? Can the squid axon regulate its cell volume? If so, is the Na,K,Cl transporter directly involved? Thus, the squid axon remains a fruitful preparation to study a transport mechanism similar to that found in a variety of cells. Its large size confers unique experimental advantages that should help us in our quest to understand this widely distributed transport mechanism.     

Towards a ‘Sea‐Level Sensitive’ dynamic model: impact of island ontogeny and glacio‐eustasy on global patterns of marine island biogeography

A synthetic model is presented to enlarge the evolutionary framework of the General Dynamic Model (GDM) and the Glacial Sensitive Model (GSM) of oceanic island biogeography from the terrestrial to the marine realm. The proposed ‘Sea‐Level Sensitive’ dynamic model (SLS) of marine island biogeography integrates historical and ecological biogeography with patterns of glacio‐eustasy, merging concepts from areas as diverse as taxonomy, biogeography, marine biology, volcanology, sedimentology, stratigraphy, palaeontology, geochronology and geomorphology. Fundamental to the SLS model is the dynamic variation of the littoral area of volcanic oceanic islands (defined as the area between the intertidal and the 50‐m isobath) in response to sea‐level oscillations driven by glacial–interglacial cycles. The following questions are considered by means of this revision: (i) what was the impact of (global) glacio‐eustatic sea‐level oscillations, particularly those of the Pleistocene glacial–interglacial episodes, on the littoral marine fauna and flora of volcanic oceanic islands? (ii) What are the main factors that explain the present littoral marine biodiversity on volcanic oceanic islands? (iii) How can differences in historical and ecological biogeography be reconciled, from a marine point of view? These questions are addressed by compiling the bathymetry of 11 Atlantic archipelagos/islands to obtain quantitative data regarding changes in the littoral area based on Pleistocene sea‐level oscillations, from 150 thousand years ago (ka) to the present. Within the framework of a model sensitive to changing sea levels, we discuss the principal factors affecting the geographical range of marine species; the relationships between modes of larval development, dispersal strategies and geographical range; the relationships between times of speciation, modes of larval development, ecological zonation and geographical range; the influence of sea‐surface temperatures and latitude on littoral marine species diversity; the effect of eustatic sea‐level changes and their impact on the littoral marine biota; island marine species–area relationships; and finally, the physical effects of island ontogeny and its associated submarine topography and marine substrate on littoral biota. Based on the SLS dynamic model, we offer a number of predictions for tropical, subtropical and temperate volcanic oceanic islands on how rates of immigration, colonization, in‐situ speciation, local disappearance, and extinction interact and affect the marine biodiversity around islands during glacials and interglacials, thus allowing future testing of the theory.     

Herbivorous insects: model systems for the comparative study of speciation ecology

Does ecological divergence drive species-level evolutionary diversification? How so and to what degree? These questions were central to the thinking of the evolutionary synthesis. Only recently, however, has the ecology of speciation become an important focus of empirical study. Here, we argue that ecologically specialized, phylogenetically diverse, and experimentally tractable herbivorous insect taxa offer great opportunities to study the myriad mechanisms by which ecology may cause reproductive isolation and promote speciation. We call for the development and integrated experimental study of a taxonomic diversity of herbivore model systems and discuss the availability and recent evaluation of suitable taxa. Most importantly, we describe a general comparative framework that can be used to rigorously test a variety of hypotheses about the relative contributions and the macroevolutionary generality of particular mechanisms. Finally, we illustrate important issues for the experimental analysis of speciation ecology by demonstrating the consequences of specialized host associations for ecological divergence and premating isolation in Neochlamisus bebbianae leaf beetles.     

Laboratory environments are not conducive for allopatric speciation

We review published records of laboratory experiments on peripatric and vicariance allopatric speciation to address the following three questions: (1) What was the true effect size of reproductive isolation? (2) Was the reproductive isolation persistent? (3) What influenced the development of isolation? Contrary to popular belief, laboratory evidence for allopatric speciation is quite weak. Assortative mating was only found among derived populations in vicariance experiments. Reproductive isolation against control populations was only intermittent, so there is reason to doubt if some cases showing significant reproductive isolation really should be attributed to speciation. The method of testing was at least as important as the speciation model. Experimental populations tested against each other were the most likely to demonstrate reproductive isolation. This study suggests that allopatric speciation experiments are more likely to yield conclusive results under divergent selection than under drift, and points to the benefits of large populations and many generations.     

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.     

A Phylogenomic Approach to Vertebrate Phylogeny Supports a Turtle-Archosaur Affinity and a Possible Paraphyletic Lissamphibia

In resolving the vertebrate tree of life, two fundamental questions remain: 1) what is the phylogenetic position of turtles within amniotes, and 2) what are the relationships between the three major lissamphibian (extant amphibian) groups? These relationships have historically been difficult to resolve, with five different hypotheses proposed for turtle placement, and four proposed branching patterns within Lissamphibia. We compiled a large cDNA/EST dataset for vertebrates (75 genes for 129 taxa) to address these outstanding questions. Gene-specific phylogenetic analyses revealed a great deal of variation in preferred topology, resulting in topologically ambiguous conclusions from the combined dataset. Due to consistent preferences for the same divergent topologies across genes, we suspected systematic phylogenetic error as a cause of some variation. Accordingly, we developed and tested a novel statistical method that identifies sites that have a high probability of containing biased signal for a specific phylogenetic relationship. After removing putatively biased sites, support emerged for a sister relationship between turtles and either crocodilians or archosaurs, as well as for a caecilian-salamander sister relationship within Lissamphibia, with Lissamphibia potentially paraphyletic.     

Population growth rate as a basis for ecological risk assessment of toxic chemicals

Assessing the ecological risks of toxic chemicals is most often based on individual-level responses such as survival, reproduction or growth. Such an approach raises the following questions with regard to translating these measured effects into likely impacts on natural populations. (i) To what extent do individual-level variables underestimate or overestimate population-level responses? (ii) How do toxicant-caused changes in individual-level variables translate into changes in population dynamics for species with different life cycles? (iii) To what extent are these relationships complicated by population-density effects? These issues go to the heart of the ecological relevance of ecotoxicology and we have addressed them using the population growth rate as an integrating concept. Our analysis indicates that although the most sensitive individual-level variables are likely to be equally or more sensitive to increasing concentrations of toxic chemicals than population growth rate, they are difficult to identify a priori and, even if they could be identified, integrating impacts on key life-cycle variables via population growth rate analysis is nevertheless a more robust approach for assessing the ecological risks of chemicals. Populations living under density-dependent control may respond differently to toxic chemicals than exponentially growing populations, and greater care needs to be given to incorporating realistic density conditions (either experimentally or by simulation) into ecotoxicological test designs. It is impractical to expect full life-table studies, which record changes in survival, fecundity and development at defined intervals through the life cycle of organisms under specified conditions, for all relevant species, so we argue that population growth rate analysis should be used to provide guidance for a more pragmatic and ecologically sound approach to ecological risk assessment.     

Native versus exotic community patterns across three scales: Roles of competition,environment and incomplete invasion

Three fundamental, interrelated questions in invasion ecology are: (1) to what extent do exotic species outcompete natives; (2) are native and exotic communities functionally similar or different; and (3) are differences in biogeographic patterns in native and exotic communities due to incomplete invasions among exotics? These questions are analogous to general questions in community ecology regarding the relative roles of competition, environmental response and dispersal limitation in community assembly. We addressed each of these questions for plant communities in discrete meadow patches, using analyses at three scales ranging from the landscape to microsites. A weak positive relationship between native and exotic species richness in microsites, and a predominance of positive correlations in abundance among native and exotic species pairs suggest that competition has been less important than other factors in determining native versus exotic abundance and community composition. In contrast, models of species richness and community compositional change across scales suggest native versus exotic community patterns are largely determined by a mix of scale-dependent concordant (shared positive or negative) and discordant relationships with environmental variables. In addition, detailed analyses of species-area and species-abundance relationships suggest ongoing expansion of exotic species populations, indicating that the assembly of the exotic community is in its early stages. Thus, while competition does not appear to strongly affect native versus exotic abundances and compositions at present, it may intensify in the future. Our results indicate that synoptic patterns in native versus exotic richness that have been previously attributed to a single cause may in fact be due to a complex mix of concordant and discordant responses to environmental factors across scales. They also suggest that conservation efforts aimed at promoting natives and reducing exotics should focus on the factors and scales for which such a response (i.e., promotion of high native and low exotic richness) can be expected.     

Recovering speciation and extinction dynamics based on phylogenies

Phylogenetic trees of only extant species contain information about the underlying speciation and extinction pattern. In this review, I provide an overview over the different methodologies that recover the speciation and extinction dynamics from phylogenetic trees. Broadly, the methods can be divided into two classes: (i) methods using the phylogenetic tree shapes (i.e. trees without branch length information) allowing us to test for speciation rate variation and (ii) methods using the phylogenetic trees with branch length information allowing us to quantify speciation and extinction rates. I end the article with an overview on limitations, open questions and challenges of the reviewed methodology.     

Impacts of climate warming on hybrid zone movement: Geographically diffuse and biologically porous “species borders”

Abstract The ecology and evolutionary biology of insect–plant associations has realized extensive attention, especially during the past 60 years. The classifications (categorical designations) of continuous variation in biodiversity, ranging from global patterns (e.g., latitudinal gradients in species richness/diversity and degree of herbivore feeding specialization) to localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious. Semantic and biosystematic (taxonomical) disagreements sometimes detract from more important ecological and evolutionary processes that drive diversification, the dynamics of gene flow and local extinctions. This review addresses several aspects of insect specialization, host‐associated divergence and ecological (including “hybrid”) speciation, with special reference to the climate warming impacts on species borders of hybridizing swallowtail butterflies (Papilionidae). Interspecific hybrid introgression may result in collapse of multi‐species communities or increase species numbers via homoploid hybrid speciation. We may see diverging, merging, or emerging genotypes across hybrid zones, all part of the ongoing processes of evolution. Molecular analyses of genetic mosaics and genomic dynamics with “divergence hitchhiking”, combined with ecological, ethological and physiological studies of “species porosity”, have already begun to unveil some answers for some important ecological/evolutionary questions. (i) How rapidly can host‐associated divergence lead to new species (and why doesn't it always do so, e.g., resulting in “incomplete” speciation)? (ii) How might “speciation genes” function, and how/where would we find them? (iii) Can oscillations from specialists to generalists and back to specialists help explain global diversity in herbivorous insects? (iv) How could recombinant interspecific hybridization lead to divergence and speciation? From ancient phytochemically defined angiosperm affiliations to recent and very local geographical mosaics, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of ecological patterns and evolutionary processes, including host‐associated genetic divergence, genomic mosaics, genetic hitchhiking and sex‐linked speciation genes. Apparent homoploid hybrid speciation in Papilio appears to have been catalyzed by climate warming‐induced interspecific introgression of some, but not all, species diagnostic traits, reflecting strong divergent selection (discordant), especially on the Z (= X) chromosome. Reproductive isolation of these novel recombinant hybrid genotypes appears to be accomplished via a delayed post‐diapause emergence or temporal isolation, and is perhaps aided by the thermal landscape. Changing thermal landscapes appear to have created (and may destroy) novel recombinant hybrid genotypes and hybrid species.     

Nuclear and mitochondrial phylogeography of the Atlantic forest endemic Xiphorhynchus fuscus (Aves: Dendrocolaptidae): biogeography and systematics implications

We studied the intraspecific evolutionary history of the South American Atlantic forest endemic Xiphorhynchusfuscus (Aves: Dendrocolaptidae) to address questions such as: Was the diversification of this bird's populations associated to areas of avian endemism? Which models of speciation (i.e., refuges, river as barriers or geotectonism) explain the diversification within X. fuscus? Does the genetic data support subspecies as independent evolutionary units (species)? We used mitochondrial (n=34) and nuclear (n=68) DNA sequences of X. fuscus to study temporal and spatial relationships within and between populations. We described four main monophyletic lineages that diverged during the Pleistocene. The subspecies taxonomy did not match all the evolutionary lineages; subspecies atlanticus was the only one that represented a monophyletic and isolated lineage. The distribution of these lineages coincided with some areas of endemism for passerines, suggesting that those areas could be regions of biotic differentiation. The ancestor of X. fuscus diverged approximately 3 million years ago from Amazonian taxa and the phylogeographic pattern suggested that X. fuscus radiated from northeastern Brazil. Neither the riverine nor the geotectonic vicariance models are supported as the primary cause for diversification of geographic lineages, but rainforest contractions and expansions (ecological vicariance) can explain most of the spatial divergence observed in this species. Finally, analyses of gene flow and divergence time estimates suggest that the endangered subspecies atlanticus (from northeastern Brazil) can be considered a full species under the general lineage species concept.     

Dynamics of speciation and diversification in a metapopulation

We develop a simple framework for modeling speciation and diversification as a continuous process of accumulation of genetic (or morphological) differences accompanied by species and subpopulation extinction and/or range expansion. This framework can be used to approach a number of questions such as species-area distribution, species-range size distribution, the rate of ecological turnover, asymmetries of range division between sister species, waiting time until speciation and extinction, the relationship between the geographic range size and the probability of speciation, the relationships between subpopulation-level parameters and metapopulation-level parameters, and the effects of taxonomic level on these rates, distributions, and parameters. We illustrate some of these applications using numerical simulations. We develop approximations describing the dependence of the number of different taxonomic units, their average range size, and the rate of their turnover on the system size, the rate of fixation of genetic (or morphological) changes in local demes, and the rate of local extinction and colonization.