The genetic architecture of hybrid incompatibilities and their effect on barriers to introgression in secondary contact

Genetic incompatibilities are an important component of reproductive isolation. Although theoretical studies have addressed their evolution, little is known about their maintenance when challenged by potentially high migration rates in secondary contact. Although theory predicts that recombination can erode barriers, many empirical systems have been found to retain species‐specific differences despite substantial gene flow. By simulating whole genomes in individuals of hybridizing species, we find that the genetic architecture of two contrasting models of epistatic hybrid incompatibilities and the context of hybridization can substantially affect species integrity and genomic heterogeneity. In line with theory, our results show that intergenomic incompatibilities break down rapidly by recombination, but can maintain genome‐wide differentiation under very limited conditions. By contrast, intragenomic interactions that arise from genetic pathways can maintain species‐specific differences even with high migration rates and gene flow, whereas introgression at large parts of the genome can simultaneously remain extensive, consistent with empirical observations. We discuss the importance of intragenomic interactions in speciation and consider how this form of epistatic fitness variation is implicated and supported by other theoretical and empirical studies. We further address the relevance of replicates and knowledge of context when investigating the genomics of speciation.     

ESTIMATING SPECIATION AND EXTINCTION RATES FROM DIVERSITY DATA AND THE FOSSIL RECORD

Understanding the processes that underlie biodiversity requires insight into the evolutionary history of the taxa involved. Accurate estimation of speciation, extinction, and diversification rates is a prerequisite for gaining this insight. Here, we develop a stochastic birth–death model of speciation and extinction that predicts the probability distribution of both extinct and extant numbers of species in a clade. We present two estimation methods based on this model given data on the number of extinct species (from the fossil record) and extant species (from diversity assessments): a multivariate method of moments approach and a maximum-likelihood approach. We show that, except for some special cases, the two estimation methods produce very similar estimates. This is convenient, because the usually preferred maximum-likelihood approach is much more computationally demanding, so the method of moments can serve as a proxy. Furthermore, we introduce a correction for possible bias that can arise by the mere fact that we will normally only consider extant clades. We find that in some cases the bias correction affects the estimates profoundly. Finally, we show how our model can be extended to incorporate incomplete preservation. Preservation rates can, however, not be reliably estimated on the basis of numbers of extant and extinct species alone.     

PHYLOGENETIC ANALYSIS OF TRAIT EVOLUTION AND SPECIES DIVERSITY VARIATION AMONG ANGIOSPERM FAMILIES

Angiosperm families differ greatly from one another in species richness (S). Previous studies have attributed significant components of this variation to the influence of pollination mode (biotic/abiotic) and growth form (herbaceous/woody) on speciation rate, but these results suffer difficulties of interpretation because all the studies ignored the phylogenetic relationships among families. We use a molecular phylogeny of the angiosperm families to reanalyse correlations between S and family-level traits and use reconstructions of trait evolution to interpret the results. We confirm that pollination mode and growth form are correlated with S and show that the majority of changes in pollination mode involved a change from biotic to abiotic pollination with an associated fall in speciation rate. The majority of growth form changes involved the evolution of herbaceousness from woodiness with a correlated rise in speciation rate. We test the hypothesis of Ricklefs and Renner (1994) that “evolutionary flexibility” rather than other trait changes triggered increased speciation rates in some families, but find little support for the hypothesis.     

How likely is speciation in neutral ecology?

Patterns of biodiversity predicted by the neutral theory rely on a simple phenomenological model of speciation. To further investigate the effect of speciation on neutral biodiversity, we analyze a spatially explicit neutral model based on population genetics. We define the metacommunity as a system of populations exchanging migrants, and we use this framework to introduce speciation with little or no gene flow (allopatric and parapatric speciation). We find that with realistic mutation rates, our metacommunity model driven by neutral processes cannot support more than a few species. Adding natural selection in the population genetics of speciation increases the number of species in the metacommunity, but the level of diversity found in the Barro Colorado Island is difficult to reach.     

Scale and species numbers

One of the main tasks confronting community ecologists is to explain why a particular site harbours a certain number of species. The site might range from a drop of water to the whole Earth, and the species might be drawn from a very restricted taxon or include all living organisms. The common problem, however, is to understand the relative importance of speciation and extinction and, more locally, of immigration and loss. Speciation is the ultimate motor driving biodiversity and ecologists need to know the factors influencing rates of speciation, and whether there is a feedback, positive or negative, between species numbers and the generation of new taxa. However, the relative importance of speciation and other factors determining species numbers varies crucially across different scales of enquiry. Here, we explore some of these issues as we move from a macro- to microscale perspective, focusing on a limited number of studies that we believe make important advances in the field.     

Larval habits, host-plant associations, and speciation in nematine sawflies (Hymenoptera: Tenthredinidae)

Adaptive radiations consist of two intertwined processes, diversification of species and diversification of their ecological niches, but it is unclear whether there is a causal link between the processes. In phytophagous insects, ecological diversification mainly involves shifts in host-plant associations and in larval feeding habits (internal or external) on different plant parts, and several observations indicate that speciation is facilitated by host shifts. Data on host use in individual species suggest that internal feeders are less likely to colonize new hosts than external-feeding taxa and, consequently, increases in collective host ranges and species numbers should be slowed down in endophagous lineages. We tested these related hypotheses by using phylogenetic information to reconstruct the evolutionary history of larval resource use in the sawfly subfamily Nematinae, a group of 1000 plus species with a broad range of niches: the subfamily's combined host range includes over 20 plant families, and larvae may feed externally on leaves or needles, or internally, for example, in buds, fruits, leaves, or galls. The results show that: (1) Most internally feeding groups have evolved independently from external-feeding ancestors, but several distinct internal habits have appeared convergently multiple times; (2) Shifts among host taxa are clearly more common than changes in larval habits; (3) The majority of host switches have occurred among phylogenetically close plant groups, but many shifts are manifest among distantly related, ecologically proximate hosts; (4) Although external feeding characteristic of the common ancestor of Nematinae is associated with relatively high rates of host-shifting, internal feeders are very conservative in their host use; (5) In contrast, the effect of endophagy on speciation probabilities is more variable: net speciation rates are lowered in most internal-feeding groups, but a striking exception is found in species that induce galls on Salicaceae. The loose connection between collective host ranges and species diversity provides empirical support for theoretical models suggesting that speciation rates are a function of a complex interplay between "intrinsic" niche width and resource heterogeneity.     

Detecting local diversity‐dependence in diversification

Whether there are ecological limits to species diversification is a hotly debated topic. Molecular phylogenies show slowdowns in lineage accumulation, suggesting that speciation rates decline with increasing diversity. A maximum‐likelihood (ML) method to detect diversity‐dependent (DD) diversification from phylogenetic branching times exists, but it assumes that diversity‐dependence is a global phenomenon and therefore ignores that the underlying species interactions are mostly local, and not all species in the phylogeny co‐occur locally. Here, we explore whether this ML method based on the nonspatial diversity‐dependence model can detect local diversity‐dependence, by applying it to phylogenies, simulated with a spatial stochastic model of local DD speciation, extinction, and dispersal between two local communities. We find that type I errors (falsely detecting diversity‐dependence) are low, and the power to detect diversity‐dependence is high when dispersal rates are not too low. Interestingly, when dispersal is high the power to detect diversity‐dependence is even higher than in the nonspatial model. Moreover, estimates of intrinsic speciation rate, extinction rate, and ecological limit strongly depend on dispersal rate. We conclude that the nonspatial DD approach can be used to detect diversity‐dependence in clades of species that live in not too disconnected areas, but parameter estimates must be interpreted cautiously.     

Modes of speciation and the neutral theory of biodiversity

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

Asymmetry in species regional dispersal ability and the neutral theory

The neutral assumption that individuals of either the same or different species share exactly the same birth, death, migration, and speciation probabilities is fundamental yet controversial to the neutral theory. Several theoretical studies have demonstrated that a slight difference in species per capita birth or death rates can have a profound consequence on species coexistence and community structure. Whether asymmetry in migration, a vital demographic parameter in the neutral model, plays an important role in community assembly still remains unknown. In this paper, we relaxed the ecological equivalence assumption of the neutral model by introducing differences into species regional dispersal ability. We investigated the effect of asymmetric dispersal on the neutral local community structure. We found that per capita asymmetric dispersal among species could reduce species richness of the local community and result in deviations of species abundance distributions from those predicted by the neutral model. But the effect was moderate compared with that of asymmetries in birth or death rates, unless very large asymmetries in dispersal were assumed. A large difference in species dispersal ability, if there is, can overwhelm the role of random drift and make local community dynamics deterministic. In this case, species with higher regional dispersal abilities tended to dominate in the local community. However, the species abundance distribution of the local community under asymmetric dispersal could be well fitted by the neutral model, but the neutral model generally underestimated the fundamental biodiversity number but overestimated the migration rate in such communities.     

Linking population‐level and microevolutionary processes to understand speciation dynamics at the macroevolutionary scale

Although speciation dynamics have been described for several taxonomic groups in distinct geographic regions, most macroevolutionary studies still lack a detailed mechanistic view on how or why speciation rates change. To help partially fill this gap, we suggest that the interaction between the time taken by a species to geographically expand and the time populations take to evolve reproductive isolation should be considered when we are trying to understand macroevolutionary patterns. We introduce a simple conceptual index to guide our discussion on how demographic and microevolutionary processes might produce speciation dynamics at macroevolutionary scales. Our framework is developed under different scenarios: when speciation is mediated by geographical or resource‐partitioning opportunities, and when diversity is limited or not. We also discuss how organismal intrinsic properties and different overall geographical settings can influence the tempo and mode of speciation. We argue that specific conditions observed at the microscale might produce a pulse in speciation rates even without a pulse in either climate or physical barriers. We also propose a hypothesis to reconcile the apparent inconsistency between speciation measured at the microscale and macroscale, and emphasize that diversification rates are better seen as an emergent property. We hope to bring the reader''s attention to interesting mechanisms to be further studied, to motivate the development of new theoretical models that connect microevolution and macroevolution, and to inspire new empirical and methodological approaches to more adequately investigate speciation dynamics either using neontological or paleontological data.     

Hidden histories of gene flow in highland birds revealed with genomic markers

Genomic studies are revealing that divergence and speciation are marked by gene flow, but it is not clear whether gene flow has played a prominent role during the generation of biodiversity in species‐rich regions of the world where vicariance is assumed to be the principal mode by which new species form. We revisit a well‐studied organismal system in the Mexican Highlands, Aphelocoma jays, to test for gene flow among Mexican sierras. Prior results from mitochondrial DNA (mtDNA) largely conformed to the standard model of allopatric divergence, although there was also evidence for more obscure histories of gene flow in a small sample of nuclear markers. We tested for these ‘hidden histories’ using genomic markers known as ultraconserved elements (UCEs) in concert with phylogenies, clustering algorithms and newer introgression tests specifically designed to detect ancient gene flow (e.g. ABBA/BABA tests). Results based on 4303 UCE loci and 2500 informative SNPs are consistent with varying degrees of gene flow among highland areas. In some cases, gene flow has been extensive and recent (although perhaps not ongoing today), whereas in other cases there is only a trace signature of ancient gene flow among species that diverged as long as 5 million years ago. These results show how a species complex thought to be a model for vicariance can reveal a more reticulate history when a broader portion of the genome is queried. As more organisms are studied with genomic data, we predict that speciation‐with‐bouts‐of‐gene‐flow will turn out to be a common mode of speciation.     

Inferring the Dynamics of Diversification: A Coalescent Approach

Recent analyses of the fossil record and molecular phylogenies suggest that there are fundamental limits to biodiversity, possibly arising from constraints in the availability of space, resources, or ecological niches. Under this hypothesis, speciation rates decay over time and biodiversity eventually saturates, with new species emerging only when others are driven to extinction. This view of macro-evolution contradicts an alternative hypothesis that biodiversity is unbounded, with species ever accumulating as they find new niches to occupy. These contrasting theories of biodiversity dynamics yield fundamentally different explanations for the disparity in species richness across taxa and regions. Here, we test whether speciation rates have decayed or remained constant over time, and whether biodiversity is saturated or still expanding. We first derive a general likelihood expression for internode distances in a phylogeny, based on the well-known coalescent process from population genetics. This expression accounts for either time-constant or time-variable rates, time-constant or time-variable diversity, and completely or incompletely sampled phylogenies. We then compare the performance of different diversification scenarios in explaining a set of 289 phylogenies representing amphibians, arthropods, birds, mammals, mollusks, and flowering plants. Our results indicate that speciation rates typically decay over time, but that diversity is still expanding at present. The evidence for expanding-diversity models suggests that an upper limit to biodiversity has not yet been reached, or that no such limit exists.     

Biodiversity loss through speciation collapse: Mechanisms,warning signals,and possible rescue*

Speciation is the process that generates biodiversity, but recent empirical findings show that it can also fail, leading to the collapse of two incipient species into one. Here, we elucidate the mechanisms behind speciation collapse using a stochastic individual‐based model with explicit genetics. We investigate the impact of two types of environmental disturbance: deteriorated visual conditions, which reduce foraging ability and impede mate choice, and environmental homogenization, which restructures ecological niches. We find that: (1) Species pairs can collapse into a variety of forms including new species pairs, monomorphic or polymorphic generalists, or single specialists. Notably, polymorphic generalist forms may be a transient stage to a monomorphic population; (2) Environmental restoration enables species pairs to reemerge from single generalist forms, but not from single specialist forms; (3) Speciation collapse is up to four orders of magnitude faster than speciation, while the reemergence of species pairs can be as slow as de novo speciation; (4) Although speciation collapse can be predicted from either demographic, phenotypic, or genetic signals, observations of phenotypic changes allow the most general and robust warning signal of speciation collapse. We conclude that factors altering ecological niches can reduce biodiversity by reshaping the ecosystem's evolutionary attractors.     

Speciation-rate dependence in species–area relationships

The general tendency for species number (S) to increase with sampled area (A) constitutes one of the most robust empirical laws of ecology, quantified by species–area relationships (SAR). In many ecosystems, SAR curves display a power-law dependence, S∝A^z. The exponent z is always less than one but shows significant variation in different ecosystems. We study the multitype voter model as one of the simplest models able to reproduce SAR similar to those observed in real ecosystems in terms of basic ecological processes such as birth, dispersal and speciation. Within the model, the species–area exponent z depends on the dimensionless speciation rate ν, even though the detailed dependence is still matter of controversy. We present extensive numerical simulations in a broad range of speciation rates from ν=10^-3 down to ν=10^-11, where the model reproduces values of the exponent observed in nature. In particular, we show that the inverse of the species–area exponent linearly depends on the logarithm of ν. Further, we compare the model outcomes with field data collected from previous studies, for which we separate the effect of the speciation rate from that of the different species lifespans. We find a good linear relationship between inverse exponents and logarithm of species lifespans. However, the slope sets bounds on the speciation rates that can hardly be justified on evolutionary basis, suggesting that additional effects should be taken into account to consistently interpret the observed exponents.     

How phenotypic matching based on neutral mating cues enables speciation in locally adapted populations

Maynard Smith's (American Naturalist, 1966, 100, 637) suggestion that in some cases a prerequisite for speciation is the existence of local ecological adaptations has not received much attention to date. Here, we test the hypothesis using a model like that of Maynard Smith but differing in the way animals disperse between niches. In previous studies, males disperse randomly between niches but females stay put in their natal niche. As a first step toward generalizing the model, we here analyze the case that equal proportions of the two sexes disperse between niches before breeding. Supporting Maynard Smith's (1966) hypothesis, we find that once local adaptations are established, a neutral mating cue at an independent locus can rapidly enable speciation in populations with a suitable mechanism for phenotype matching. We find that stable ecological polymorphisms are relatively insensitive to the strength of selection, but depend crucially on the extent of dispersal between niches, with a threshold of ~5% if population sizes in two niches are equal. At higher levels of dispersal, ecological differentiation is lost. These results contrast with those of earlier studies and shed light on why parapatric speciation is limited by the extent of gene flow. Our testable model provides a candidate explanation for the rapid speciation rates, diversity of appearance and occurrence of “species flocks” observed among some African cichlids and neotropical birds and may also have implications for the occurrence of punctuational change on phylogenies.     

Process-based species delimitation leads to identification of more biologically relevant species*

Most approaches to species delimitation to date have considered divergence-only models. Although these models are appropriate for allopatric speciation, their failure to incorporate many of the population-level processes that drive speciation, such as gene flow (e.g., in sympatric speciation), places an unnecessary limit on our collective understanding of the processes that produce biodiversity. To consider these processes while inferring species boundaries, we introduce the R-package delimitR and apply it to identify species boundaries in the reticulate taildropper slug (Prophysaon andersoni). Results suggest that secondary contact is an important mechanism driving speciation in this system. By considering process, we both avoid erroneous inferences that can be made when population-level processes such as secondary contact drive speciation but only divergence is considered, and gain insight into the process of speciation in terrestrial slugs. Further, we apply delimitR to three published empirical datasets and find results corroborating previous findings. Finally, we evaluate the performance of delimitR using simulation studies, and find that error rates are near zero when comparing models that include lineage divergence and gene flow for three populations with a modest number of Single Nucleotide Polymorphisms (SNPs; 1500) and moderate divergence times (<100,000 generations). When we apply delimitR to a complex model set (i.e., including divergence, gene flow, and population size changes), error rates are moderate (∼0.15; 10,000 SNPs), and, when present, misclassifications occur among highly similar models.     

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.     

Phylogenetic inference of reciprocal effects between geographic range evolution and diversification

Geographic characters--traits describing the spatial distribution of a species-may both affect and be affected by processes associated with lineage birth and death. This is potentially confounding to comparative analyses of species distributions because current models do not allow reciprocal interactions between the evolution of ranges and the growth of phylogenetic trees. Here, we introduce a likelihood-based approach to estimating region-dependent rates of speciation, extinction, and range evolution from a phylogeny, using a new model in which these processes are interdependent. We demonstrate the method with simulation tests that accurately recover parameters relating to the mode of speciation and source-sink dynamics. We then apply it to the evolution of habitat occupancy in Californian plant communities, where we find higher rates of speciation in chaparral than in forests and evidence for expanding habitat tolerances.