Phylogenetics and speciation

Species-level phylogenies derived from molecular data provide an indirect record of the speciation events that have led to extant species. This offers enormous potential for investigating the general causes and rates of speciation within clades. To make the most of this potential, we should ideally sample all the species in a higher group, such as a genus, ensure that those species reflect evolutionary entities within the group, and rule out the effects of other processes, such as extinction, as explanations for observed patterns. We discuss recent practical and theoretical advances in this area and outline how future work should benefit from incorporating data from genealogical and phylogeographical scales.     

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.     

Pleistocene speciation is not refuge speciation

A number of researchers working on the origin of extant Neotropical biodiversity implicitly and without appropriate proofs assume that Pleistocene speciation should necessarily follow the rules of the refuge hypothesis. A recent example is provided by a study of Neotropical butterflies. Although the analysis showed that these groups experienced their main diversification burst during the last 2.6 million years, coinciding with the Pleistocene glacial cycles (Garzón‐Orduña et al., 2014, Journal of Biogeography, 41 , 1631–1638), a causal link between the speciation chronology and the evolutionary mechanisms proposed by the refuge hypothesis is not provided. Without more detailed studies on the environmental drivers, geographical patterns and speciation modes, establishing a causal link between speciation chronology and a particular speciation model – of which the refuge hypothesis is only one among many possibilities – is too speculative. Here I provide a six‐step conceptual framework for linking the speciation chronology with the environmental drivers and the ecological and evolutionary mechanisms potentially involved.     

Population genomics and speciation

The process of speciation begins with genomically-localised barriers to gene exchange associated with loci for local adaptation, intrinsic incompatibility or assortative mating. The barrier then spreads until reproductive isolation influences the whole genome. The population genomics approach can be used to identify regions of reduced gene flow by detecting loci with greater differentiation than expected from the average across many loci. Recently, this approach has been used in several systems. I review these studies, concentrating on the robustness of the approach and the methods available to go beyond the simple identification of differentiated markers. Population genomics has already contributed significantly to understanding the balance between gene flow and selection during the evolution of reproductive isolation and has great future potential both in genome species and in non-model organisms.     

Fungal evolution and speciation

Molecular-genetic methods are making possible a revolution in the the study of fungal evolutionary biology. To date, substantial progress has been made toward the goal of determining phylogenetic relationships, This is particularly true for higher taxonomic levels, where small-subunit rRNA sequences have proved valuable. The tremendous range of life-cycle diversity exhibited among fungi makes them excellent candidates for exploring areas of evolutionary biology that are as yet poorly investigated, particularly in terms of population biology, reproductive strategies and speciation. This argument is supported by the results of recent studies.     

Chromosomal rearrangements and speciation

Several authors have proposed that speciation frequently occurs when a population becomes fixed for one or more chromosomal rearrangements that reduce fitness when they are heterozygous. This hypothesis has little theoretical support because mutations that cause a large reduction in fitness can be fixed through drift only in small, inbred populations. Moreover, the effects of chromosomal rearrangements on fitness are unpredictable and vary significantly between plants and animals. I argue that rearrangements reduce gene flow more by suppressing recombination and extending the effects of linked isolation genes than by reducing fitness. This unorthodox perspective has significant implications for speciation models and for the outcomes of contact between neospecies and their progenitor(s).     

Bacterial species and speciation

Bacteria are profoundly different from eukaryotes in their patterns of genetic exchange. Nevertheless, ecological diversity is organized in the same way across all of life: individual organisms fall into more less discrete clusters on the basis of their phenotypic, ecological, and DNA sequence characteristics. Each sequence cluster in the bacterial world appears to correspond to an "ecotype," defined as a population of cells in the same ecological niche, which would all be out-competed by any adaptive mutant coming from the population. Ecotypes, so defined, share many of the dynamic properties attributed to eukaryotic species: genetic diversity within an ecotype is limited by a force of cohesion (in this case, periodic selection); different ecotypes are free to diverge without constraint from one another; and ecotypes are ecologically distinct. Also, ecotypes can be discovered and classified as DNA sequence clusters, even when we are ignorant of their ecology. Owing to the rarity and promiscuity of bacterial genetic exchange, speciation in the bacterial world is expected to be much less constrained than in the world of animals and plants.     

Sexual selection and speciation

The power of sexual selection to drive changes in mate recognition traits gives it the potential to be a potent force in speciation. Much of the evidence to support this possibility comes from comparative studies that examine differences in the number of species between clades that apparently differ in the intensity of sexual selection. We argue that more detailed studies are needed, examining extinction rates and other sources of variation in species richness. Typically, investigations of extant natural populations have been too indirect to convincingly conclude speciation by sexual selection. Recent empirical work, however, is beginning to take a more direct approach and rule out confounding variables.     

Species concept and speciation

Defining and recognizing a species has been a controversial issue for a long time. To determine the variation and the limitation between species, many concepts have been proposed. When a taxonomist study a particular taxa, he/she must adopted a species concept and provide a species limitation to define this taxa. In this paper some of species concepts are discussed starting from the typological species concepts to the phylogenetic concept. Positive and negative aspects of these concepts are represented in addition to their application.     

Symbiont-induced speciation

Speciation induced by parasitic or mutualistic symbionts has been suggested for taxa ranging from plants to insects to monkeys. Previous models for symbiont-induced speciation have been based upon hybrid inferiority and selection for reinforcement genes. Taken on their own, however, such models have severe theoretical limitations and little empirical support. Two conditions that may favour symbiont-induced speciation are presented here: (1) interaction norms in which the outcomes of host/symbiont interactions differ between environments and (2) differential coadaptation of host and symbiont populations between environments or along an environmental gradient. Symbiont-induced speciation can be considered as one form of 'mixed-process coevolution': reciprocal evolution in which adaptation of a population of one species to a population of a second species (or coadaptation of the populations) causes the population of the second species to become reproductively isolated from other populations.     

Competitive speciation

A new mode of speciation, competitive speciation, is suggested. It assumes that fitness is depressed by the density of a phenotype's competitors, and that the adaptive landscape of phenotypes is complex. From this it follows that some intermediate forms may be fit if and only if some extreme forms are rare or absent. Subsequent to the evolution and population growth of both extreme forms, the intermediate may disappear and homogamy evolve among each of the extremes because of disruptive selection If so, sympatric speciation has occurred and niche space has been rendered into discrete segments.
The limitations of the forces leading to competitive speciation are explored. Competitive speciation is discussed in relation to stasipatric speciation and host race formation. It may be responsible for both. Finally the rates of geographical speciation and polyploidy are compared to those of competitive speciation. The latter should be almost as fast as polyploidy and may be at the root of adaptive radiation. Unlike either polyploidy or geographical speciation, competitive speciation accelerates when species diversity declines.     

Thermal adaptation and ecological speciation

Ecological speciation is defined as the emergence of reproductive isolation as a direct or indirect consequence of divergent ecological adaptation. Several empirical examples of ecological speciation have been reported in the literature which very often involve adaptation to biotic resources. In this review, we investigate whether adaptation to different thermal habitats could also promote speciation and try to assess the importance of such processes in nature. Our survey of the literature identified 16 animal and plant systems where divergent thermal adaptation may underlie (partial) reproductive isolation between populations or may allow the stable coexistence of sibling taxa. In many of the systems, the differentially adapted populations have a parapatric distribution along an environmental gradient. Isolation often involves extrinsic selection against locally maladapted parental or hybrid genotypes, and additional pre- or postzygotic barriers may be important. Together, the identified examples strongly suggest that divergent selection between thermal environments is often strong enough to maintain a bimodal genotype distribution upon secondary contact. What is less clear from the available data is whether it can also be strong enough to allow ecological speciation in the face of gene flow through reinforcement-like processes. It is possible that intrinsic features of thermal gradients or the genetic basis of thermal adaptation make such reinforcement-like processes unlikely but it is equally possible that pertinent systems are understudied. Overall, our literature survey highlights (once again) the dearth of studies that investigate similar incipient species along the continuum from initial divergence to full reproductive isolation and studies that investigate all possible reproductive barriers in a given system.     

Sexual conflict and speciation.

We review the significance of two forms of sexual conflict (different evolutionary interests of the two sexes) for genetic differentiation of populations and the evolution of reproductive isolation. Conflicting selection on the alleles at a single locus can occur in males and females if the sexes have different optima for a trait, and there are pleiotropic genetic correlations between the sexes for it. There will then be selection for sex limitation and hence sexual dimorphism. This sex limitation could break down in hybrids and reduce their fitness. Pleiotropic genetic correlations between the sexes could also affect the likelihood of mating in interpopulation encounters. Conflict can also occur between (sex-limited) loci that determine behaviour in males and those that determine behaviour in females. Reproductive isolation may occur by rapid coevolution of male trait and female mating preference. This would tend to generate assortative mating on secondary contact, hence promoting speciation. Sexual conflict resulting from sensory exploitation, polyspermy and the cost of mating could result in high levels of interpopulation mating. If females evolve resistance to make pre- and postmating manipulation, males from one population could be more successful with females from the other, because females would have evolved resistance to their own (but not to the allopatric) males. Between-locus sexual conflict could also occur as a result of conflict between males and females of different populations over the production of unfit hybrids. We develop models which show that females are in general selected to resist such matings and males to persist, and this could have a bearing on both the initial level of interpopulation matings and the likelihood that reinforcement will occur. In effect, selection on males usually acts to promote gene flow and to restrict premating isolation, whereas selection on females usually acts in the reverse direction. We review theoretical models relevant to resolution of this conflict. The winning role depends on a balance between the ''value of winning'' and ''power'' (relating to contest or armament costs): the winning role is likely to correlate with high value of winning and low costs. Sperm-ovum (or sperm-female tract) conflicts (and their plant parallels) are likely to obey the same principles. Males may typically have higher values of winning, but it is difficult to quantify ''power'', and females may often be able to resist mating more cheaply than males can force it. We tentatively predict that sexual conflict will typically result in a higher rate of speciation in ''female-win'' clades, that females will be responsible for premating isolation through reinforcement, and that ''female-win'' populations will be less genetically diverse.     

Nested biological variation and speciation

The modes of speciation that are thought to have contributed most to the generation of biodiversity require population differentiation as the initial stage in the speciation process. Consequently, a complete understanding of the mechanisms of speciation requires that the process be examined not just after speciation is complete, or nearly so, but also much earlier. Because reproductive isolation defines biological species, and it evolves slowly, study of the process may require a prohibitive span of time. Even if speciation could be observed directly, selection of populations in the process of speciation is typically difficult or impossible, because those that will ultimately undergo speciation cannot be distinguished from those that will differentiate but never assume the status of new biological species. One means of circumventing this problem is to study speciation in taxa comprising several sibling species, at least one of which exhibits extensive population differentiation. We illustrate this approach by exploring patterns of population variation in the post-glacial radiation of the threespine stickleback, Gasterosteus aculeatus. We focus on lacustrine populations and species within this complex, demonstrating parallel axes of divergence within populations, among populations and among species. The pattern that emerges is one of parallel relationships between phenotype and fitness at all three hierarchical levels, a pattern that facilitates exploration of the causes and consequences of speciation and secondary contact. A second outcome of this exploration is the observation that speciation can be the consequence of a cascade of effects, beginning with selection on trophic or other characteristics that in turn force the evolution of other population characteristics that precipitate speciation. Neither of these conclusions could have been reached without comparative studies of wild populations at several hierarchical levels, a conclusion reinforced by a brief survey of similar efforts to elucidate the process of speciation. We address the issues most likely to be resolved using this approach, and suggest that comparisons of natural variation within taxa at several hierarchical levels may substantially increase our understanding of the speciation process.     

Sex chromosomes and speciation.

Studies of reproductive isolation between animal species have shown (i) that if one sex of the hybrids between two species is sterile or inviable, it is usually the heterogametic sex (Haldane's rule), and (ii) the genes on the sex chromosomes play a particularly large role in hybrid sterility and inviability. We propose an explanation for these two observations which is based on the changes in chromosome conformation which take place during gametogenesis. These changes are far greater in sex chromosomes than in autosomes. They are also greater in the heterogametic than in the homogametic sex. We suggest that the sensitivity of hybrids of the heterogametic sex to the genetic divergence that occurs during periods of population isolation is partly the result of the failure of their sex chromosomes to undergo appropriate conformational changes. This hypothesis explains why the sex chromosomes play a disproportionate role in post-zygotic, but not in pre-zygotic, isolation, and why often only the germ line is sensitive to hybridization.