Pattern,process and geographic modes of speciation

The tradition of classifying cases of speciation into discrete geographic categories (allopatric, parapatric and sympatric) fuelled decades of fruitful research and debate. Not surprisingly, as the science has become more sophisticated, this simplistic taxonomy has become increasingly obsolete. Geographic patterns are now reasonably well understood. Sister species are rarely sympatric, implying that sympatric speciation, it its most general sense, is rare. However, sympatric speciation, even in its most restricted population genetic sense, is possible. Several case studies have demonstrated that divergence has occurred in nature without geographic barriers to gene flow. Obviously, different sets of criteria for sympatric speciation will lead to different numbers of qualifying cases. But changing the rules of nomenclature to make ‘sympatric speciation’ more or less common does not constitute scientific progress. Advances in the study of speciation have come from studies of the processes that constrain or promote divergence, and how they are affected by geography.     

Case studies and mathematical models of ecological speciation. 1. Cichlids in a crater lake

A recent study of a pair of sympatric species of cichlids in Lake Apoyo in Nicaragua is viewed as providing probably one of the most convincing examples of sympatric speciation to date. Here, we describe and study a stochastic, individual-based, explicit genetic model tailored for this cichlid system. Our results show that relatively rapid (<20,000 generations) colonization of a new ecological niche and (sympatric or parapatric) speciation via local adaptation and divergence in habitat and mating preferences are theoretically plausible if: (i) the number of loci underlying the traits controlling local adaptation, and habitat and mating preferences is small; (ii) the strength of selection for local adaptation is intermediate; (iii) the carrying capacity of the population is intermediate; and (iv) the effects of the loci influencing nonrandom mating are strong. We discuss patterns and timescales of ecological speciation identified by our model, and we highlight important parameters and features that need to be studied empirically to provide information that can be used to improve the biological realism and power of mathematical models of ecological speciation.     

Genetic and ecological divergence of a monophyletic cichlid species pair under fully sympatric conditions in Lake Ejagham, Cameroon

Although there is mounting evidence that speciation can occur under sympatric conditions, unambiguous examples from nature are rare and it is almost always possible to propose alternative allopatric or parapatric scenarios. To identify an unequivocal case of sympatric speciation it is, therefore, necessary to analyse natural settings where recent monophyletic species flocks have evolved within a small and confined spatial range. We have studied such a case with a cichlid species flock that comprises five Tilapia forms endemic to a tiny lake (Lake Ejagham with a surface area of approximately 0.49 km2) in Western Cameroon. Analysis of mitochondrial D-Loop sequences shows that the flock is very young (approximately 10(4) years) and has originated from an adjacent riverine founder population. We have focused our study on a particular pair of forms within the lake that currently appears to be in the process of speciation. This pair is characterized by an unique breeding colouration and specific morphological aspects, which can serve as synapomorphic characters to prove monophyly. It has differentiated into a large inshore and a small pelagic form, apparently as a response to differential utilization of food resources. Still, breeding and brood care occurs in overlapping areas, both in time and space. Analysis of nuclear gene flow on the basis of microsatellite polymorphisms shows a highly restricted gene flow between the forms, suggesting reproductive isolation between them. This reproductive isolation is apparently achieved by size assortative mating, although occasional mixed pairs can be observed. Our findings are congruent with recent theoretical models for sympatric speciation, which show that differential ecological adaptations in combination with assortative mating could easily lead to speciation in sympatry.     

PERSPECTIVE: MODELS OF SPECIATION: WHAT HAVE WE LEARNED IN 40 YEARS?

Theoretical studies of speciation have been dominated by numerical simulations aiming to demonstrate that speciation in a certain scenario may occur. What is needed now is a shift in focus to identifying more general rules and patterns in the dynamics of speciation. The crucial step in achieving this goal is the development of simple and general dynamical models that can be studied not only numerically but analytically as well. I review some of the existing analytical results on speciation. I first show why the classical theories of speciation by peak shifts across adaptive valleys driven by random genetic drift run into trouble (and into what kind of trouble). Then I describe the Bateson-Dobzhansky-Muller (BDM) model of speciation that does not require overcoming selection. I describe exactly how the probability of speciation, the average waiting time to speciation, and the average duration of speciation depend on the mutation and migration rates, population size, and selection for local adaptation. The BDM model postulates a rather specific genetic architecture of reproductive isolation. I then show exactly why the genetic architecture required by the BDM model should be common in general. Next I consider the multilocus generalizations of the BDM model again concentrating on the qualitative characteristics of speciation such as the average waiting time to speciation and the average duration of speciation. Finally, I consider two models of sympatric speciation in which the conditions for sympatric speciation were found analytically. A number of important conclusions have emerged from analytical studies. Unless the population size is small and the adaptive valley is shallow, the waiting time to a stochastic transition between the adaptive peaks is extremely long. However, if transition does happen, it is very quick. Speciation can occur by mutation and random drift alone with no contribution from selection as different populations accumulate incompatible genes. The importance of mutations and drift in speciation is augmented by the general structure of adaptive landscapes. Speciation can be understood as the divergence along nearly neutral networks and holey adaptive landscapes (driven by mutation, drift, and selection for adaptation to a local biotic and/or abiotic environment) accompanied by the accumulation of reproductive isolation as a by-product. The waiting time to speciation driven by mutation and drift is typically very long. Selection for local adaptation (either acting directly on the loci underlying reproductive isolation via their pleiotropic effects or acting indirectly via establishing a genetic barrier to gene flow) can significantly decrease the waiting time to speciation. In the parapatric case the average actual duration of speciation is much shorter than the average waiting time to speciation. Speciation is expected to be triggered by changes in the environment. Once genetic changes underlying speciation start, they go to completion very rapidly. Sympatric speciation is possible if disruptive selection and/or assortativeness in mating are strong enough. Sympatric speciation is promoted if costs of being choosy are small (or absent) and if linkage between the loci experiencing disruptive selection and those controlling assortative mating is strong.     

Low reproductive isolation and highly variable levels of gene flow reveal limited progress towards speciation between European river and brook lampreys

Ecologically based divergent selection is a factor that could drive reproductive isolation even in the presence of gene flow. Population pairs arrayed along a continuum of divergence provide a good opportunity to address this issue. Here, we used a combination of mating trials, experimental crosses and population genetic analyses to investigate the evolution of reproductive isolation between two closely related species of lampreys with distinct life histories. We used microsatellite markers to genotype over 1000 individuals of the migratory parasitic river lamprey (Lampetra fluviatilis) and freshwater‐resident nonparasitic brook lamprey (Lampetra planeri) distributed in 10 sympatric and parapatric population pairs in France. Mating trials, parentage analyses and artificial fertilizations demonstrated a low level of reproductive isolation between species even though size‐assortative mating may contribute to isolation. Most parapatric population pairs were strongly differentiated due to the joint effects of geographic distance and barriers to migration. In contrast, we found variable levels of gene flow between sympatric populations ranging from panmixia to moderate differentiation, which indicates a gradient of divergence with some population pairs that may correspond to alternative morphs or ecotypes of a single species and others that remain partially isolated. Ecologically based divergent selection may explain these variable levels of divergence among sympatric population pairs, but incomplete genome swamping following secondary contact could have also played a role. Overall, this study illustrates how highly differentiated phenotypes can be maintained despite high levels of gene flow that limit the progress towards speciation.     

The Maynard Smith model of sympatric speciation

The paper entitled "Sympatric speciation," which was published by John Maynard Smith in 1966, initiated the development of mathematical models aiming to identify the conditions for sympatric speciation. A part of that paper was devoted to a specific two-locus, two-allele model of sympatric speciation in a population occupying a two-niche system. Maynard Smith provided some initial numerical results on this model. Later, Dickinson and Antonovics (1973) and Caisse and Antonovics (1978) performed more extensive numerical studies on the model. Here, I report analytical results on the haploid version of the Maynard Smith model. I show how the conditions for sympatric and parapatric speciation and the levels of resulting genetic divergence and reproductive isolation are affected by the strength of disruptive selection and nonrandom mating, recombination rate, and the rates of male and female dispersal between the niches.     

Case studies and mathematical models of ecological speciation. 2. Palms on an oceanic island

A recent study of a pair of sympatric species of palms on the Lord Howe Island is viewed as providing probably one of the most convincing examples of sympatric speciation to date. Here we describe and study a stochastic, individual-based, explicit genetic model tailored for this palms system. Overall, our results show that relatively rapid (<50,000 generations) colonization of a new ecological niche, and sympatric or parapatric speciation via local adaptation and divergence in flowering periods are theoretically plausible if (i) the number of loci controlling the ecological and flowering period traits is small; (ii) the strength of selection for local adaptation is intermediate; and (iii) an acceleration of flowering by a direct environmental effect associated with the new ecological niche is present. We discuss patterns and time-scales of ecological speciation identified by our model, and we highlight important parameters and features that need to be studied empirically in order to provide information that can be used to improve the biological realism and power of mathematical models of ecological speciation.     

Habitat, isolation and the evolution of Madeiran Iandsnails

The Madeiran archipelago consists of Madeira itself, Porto Santo and the Deserta islands. On Madeira, the forest arid the coastal floral associations are so different that their faunas are effectively isolated and have undergone largely independent development. There are different faunal associations on the eastern peninsula and in the SE coastal region, which may have been separated from each other in the past. On Porto Santo, western and eastern hills have different faunas. Most observations on the fauna are compatible with evolution by allopatric speciation, consequent upon isolation on different islands or mountains, as opposed to parapatric or sympatric processes following disruptive selection. Some cases where the taxonomy is difficult to unravel may, however, indicate parapatric speciation; examples belong to the genera Discula and Heterostoma (Helicidae) and Amphorella (Ferussaciidae). Most evidence relating to species composition in communities is compatible with a balance of random immigration and extinction, rather than selective interaction, allowing clusters of similar sympatric species to accumulate. However, this impression may indicate that test procedures are insufficiently sensitive to detect interactions, and detailed ecological studies are required. Questions about speciation and distribution would be clarified if dates of divergence were established.     

The genetics and ecology of sympatric speciation: A case study

Mating occurs on the larval host plant in allRhagoletis species (Diptera: Tephritidae). We show how this attribute, when coupled with certain differences in other biological traits, strongly influences the mode of speciation. In species of thesuavis species group, host shifts have never occurred during speciation, and larvae feed in the husks of any walnut species(Juglans spp.), which are highly toxic. Taxa are allopatric or parapatric and exhibit deep phylogenetic nodes suggesting relatively ancient speciation events. Traits responsible for species and mate recognition, particularly in parapatric species, are morphologically distinct and strongly sexually dimorphic. All aspects of their biology, genetics and distribution are consistent with a slow rate of allopatric speciation followed by morphological divergence in secondary contact. In contrast, speciation in thepomonella species group has always involved a shift to a new, usually unrelated, non-toxic host, and all taxa within these groups are sympatric, monophagous and morphologically indistinguishable from one another. Phylogenetic nodes are very shallow, indicating recent sympatric speciation. Sympatric divergence is promoted by genetic variation which allows a portion of the original species to shift to a new habitat or host. Evidence suggests that changes in a few key loci responsible for host selection and fitness on a new host may initiate host shifts. By exploiting different habitats, competition for resources between diverging populations is reduced or avoided. We provide evidence that in phytophagous and parasitic insects sufficient intrinsic barriers to gene flow can evolve between sister populations as they adapt to different habitats or hosts to allow each population to establish independent evolutionary lineages in sympatry.     

Sympatric speciation by sexual selection: a critical reevaluation

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

What,if anything,is sympatric speciation?

Sympatric speciation has always fascinated evolutionary biologists, and for good reason; it pits diversifying selection directly against the tendency of sexual reproduction to homogenize populations. However, different investigators have used different definitions of sympatric speciation and different criteria for diagnosing cases of sympatric speciation. Here, we explore some of the definitions that have been used in empirical and theoretical studies. Definitions based on biogeography do not always produce the same conclusions as definitions based on population genetics. The most precise definitions make sympatric speciation an infinitesimal end point of a continuum. Because it is virtually impossible to demonstrate the occurrence of such a theoretical extreme, we argue that testing whether a case fits a particular definition is less informative than evaluating the biological processes affecting divergence. We do not deny the importance of geographical context for understanding divergence. Rather, we believe this context can be better understood by modelling and measuring quantities, such as gene flow and selection, rather than assigning cases to discrete categories like sympatric and allopatric speciation.     

Sympatric speciation by sexual selection alone is unlikely

According to Darwin, sympatric speciation is driven by disruptive, frequency-dependent natural selection caused by competition for diverse resources. Recently, several authors have argued that disruptive sexual selection can also cause sympatric speciation. Here, we use hypergeometric phenotypic and individual-based genotypic models to explore sympatric speciation by sexual selection under a broad range of conditions. If variabilities of preference and display traits are each caused by more than one or two polymorphic loci, sympatric speciation requires rather strong sexual selection when females exert preferences for extreme male phenotypes. Under this kind of mate choice, speciation can occur only if initial distributions of preference and display are close to symmetric. Otherwise, the population rapidly loses variability. Thus, unless allele replacements at very few loci are enough for reproductive isolation, female preferences for extreme male displays are unlikely to drive sympatric speciation. By contrast, similarity-based female preferences that do not cause sexual selection are less destabilizing to the maintenance of genetic variability and may result in sympatric speciation across a broader range of initial conditions. Certain groups of African cichlids have served as the exclusive motivation for the hypothesis of sympatric speciation by sexual selection. Mate choice in these fishes appears to be driven by female preferences for extreme male phenotypes rather than similarity-based preferences, and the evolution of premating reproductive isolation commonly involves at least several genes. Therefore, differences in female preferences and male display in cichlids and other species of sympatric origin are more likely to have evolved as isolating mechanisms under disruptive natural selection.     

Evolution of blind beetles in isolated aquifers: a test of alternative modes of speciation

Evidence is growing that not only allopatric but also sympatric speciation can be important in the evolution of species. Sympatric speciation has most convincingly been demonstrated in laboratory experiments with bacteria, but field-based evidence is limited to a few cases. The recently discovered plethora of subterranean diving beetle species in isolated aquifers in the arid interior of Australia offers a unique opportunity to evaluate alternative modes of speciation. This naturally replicated evolutionary experiment started 10-5 million years ago, when climate change forced the surface species to occupy geographically isolated subterranean aquifers. Using phylogenetic analysis, we determine the frequency of aquifers containing closely related sister species. By comparing observed frequencies with predictions from different statistical models, we show that it is very unlikely that the high number of sympatrically occurring sister species can be explained by a combination of allopatric evolution and repeated colonisations alone. Thus, diversification has occurred within the aquifers and likely involved sympatric, parapatric and/or microallopatric speciation.     

Speciation through competition: a critical review

We examined causes of speciation in asexual populations in both sympatry and parapatry, providing an alternative explanation for the speciation patterns reported by Dieckmann and Doebeli (1999) and Doebeli and Dieckmann (2003). Both in sympatry and parapatry, they find that speciation occurs relatively easily. We reveal that in the sympatric clonal model, the equilibrium distribution is continuous and the disruptive selection driving evolution of discrete clusters is only transient. Hence, if discrete phenotypes are to remain stable in the sympatric sexual model, there should be some source of nontransient disruptive selection that will drive evolution of assortment. We analyze sexually reproducing populations using the Bulmer's infinitesimal model and show that cost-free assortment alone leads to speciation and disruptive selection only arises when the optimal distribution cannot be matched--in this example, because the phenotypic range is limited. In addition, Doebeli and Dieckmann's analyses assumed a high genetic variance and a high mutation rate. Thus, these theoretical models do not support the conclusion that sympatric speciation is a likely outcome of competition for resources. In their parapatric model (Doebeli and Dieckmann 2003), clustering into distinct phenotypes is driven by edge effects, rather than by frequency-dependent competition.     

Parapatric divergence of sympatric morphs in a salamander: incipient speciation on Long Island?

Speciation is often categorized based on geographic modes (allopatric, parapatric or sympatric). Although it is widely accepted that species can arise in allopatry and then later become sympatrically or parapatrically distributed, patterns in the opposite direction are also theoretically possible (e.g. sympatric lineages or ecotypes becoming parapatric), but such patterns have not been shown at a macrogeographic scale. Here, we analyse genetic, climatic, ecological and morphological data and show that two typically sympatric colour morphs of the salamander Plethodon cinereus (redback and leadback) appear to have become parapatrically distributed on Long Island, New York, with pure‐redback populations in the west and pure‐leadback populations in the east (and polymorphic populations in between and on the mainland). In addition, the pure‐leadback populations in eastern Long Island are genetically, ecologically and morphologically divergent from both mainland and other Long Island populations, suggesting the possibility of incipient speciation. This parapatric separation seems to be related to the different ecological preferences of the two morphs, preferences which are present on the mainland and across Long Island. These results potentially support the idea that spatial segregation of sympatric ecotypes may sometimes play an important part in parapatric speciation.     

Phylogeny and Speciation of Felids

The phylogeny of the Felidae is reconstructed using a total evidence approach combining sequences from 12S rRNA, 16S rRNA, NADH-5, and cytochrome b genes with morphological and karyological characters. The 1504-character data set generated two equally parsimonious trees (CI = 0.413, 1795 steps) of which a strict consensus revealed one polytomy in the placement of the bay cat group. The tree supports several traditional groupings such as the genera Panthera and Lynx and the ocelot group of small South American felids, and it provides additional resolution of relationships within and among the major felid lineages. Combining phylogenetic, distributional, and ecological data indicates that vicariant speciation has played a relatively minor role in the diversification of the felids (approximately 26% of events), while sympatric speciation has been more important than expected on theoretical grounds (approximately 51.8% of events), although postspeciation dispersal may have blurred the boundaries between sympatric, parapatric, and peripheral isolate modes. An examination of ecological changes on the felid tree shows repeated patterns of resource partitioning in time (activity patterns), space (preferred habitat type), and food (as measured by body size) among closely related species. The rapid diversification of the cats thus appears to have been associated more with ecological than with geological separation.     

Adaptive sympatric speciation of polychromatic "roundfin" sailfin silverside fish in Lake Matano (Sulawesi)

The significance of sympatric speciation is one of the most controversial topics in evolutionary biology. Theory suggests that different factors can lead to speciation in full geographical contact, including selection and nonrandom mating. Strict criteria have been established for assessing sympatric speciation, which have been met in only a very few cases. Here, we investigate differentiation among sympatric morphospecies and color morphs of "roundfin" sailfin silversides (Telmatherinidae), small freshwater fish endemic to ancient Lake Matano in Central Sulawesi (Indonesia). Morphospecies are distinct according to body shape (geometric morphometrics), population structure (population-level amplified fragment length polymorphism [AFLP] markers), ecology, and mating behavior (habitat transects, stomach contents). Explorative genome scans based on AFLPs indicate that divergent selection affects only 1.3-4.2% of the analyzed loci, suggesting an early stage of speciation. Transect data demonstrate strong assortative mating and adaptive niche differentiation. However, we find no restrictions in gene flow among the conspicuous male color morphs. In summary, our data are consistent with a sympatric mode of divergence among three morphospecies under conditions effectively ruling out allopatric scenarios. Substantial, but incomplete, reproductive isolation suggests an early stage of speciation, most likely due to ecological selection pressure.     

Genetics of male nuptial colour divergence between sympatric sister species of a Lake Victoria cichlid fish

The hypothesis of sympatric speciation by sexual selection has been contentious. Several recent theoretical models of sympatric speciation by disruptive sexual selection were tailored to apply to African cichlids. Most of this work concludes that the genetic architecture of female preference and male trait is a key determinant of the likelihood of disruptive sexual selection to result in speciation. We investigated the genetic architecture controlling male nuptial colouration in a sympatric sibling species pair of cichlid fish from Lake Victoria, which differ conspicuously in male colouration and female mating preferences for these. We estimated that the difference between the species in male nuptial red colouration is controlled by a minimum number of two to four genes with significant epistasis and dominance effects. Yellow colouration appears to be controlled by one gene with complete dominance. The two colours appear to be epistatically linked. Knowledge on how male colouration segregates in hybrid generations and on the number of genes controlling differences between species can help us assess whether assumptions made in simulation models of sympatric speciation by sexual selection are realistic. In the particular case of the two sister species that we studied a small number of genes causing major differences in male colouration may have facilitated the divergence in male colouration associated with speciation.     

Cryptic barriers to dispersal within a lake allow genetic differentiation of Eurasian perch

Gene flow between coexisting or nearby populations normally prevents genetic divergence and local adaptation. Despite this, there are an increasing number of reports of sympatric sister taxa, indicating potential divergence and speciation in the face of gene flow. A large number of such reported cases involve lake-dwelling fish, which are expected to run into few physical barriers to dispersal within their aquatic habitat. However, such cases may not necessarily reflect sympatric speciation if cryptic dispersal barriers are common in lakes and other aquatic systems. In this study, we examined genetic differentiation in perch (Perca fluviatilis L.) from nine locations in a single, small lake (24 km(2)), using microsatellites. We detected significant genetic differentiation in all but two pairwise comparisons. These patterns were not consistent with divergence by distance or the existence of kin groups. Instead, they suggest that cryptic barriers to dispersal exist within the lake, allowing small-scale genetic divergence. Such an observation suggests that allopatric (or parapatric) divergence may be possible, even in small, apparently homogenous environments such as lakes. This has important consequences for how we currently view evidence from nature for sympatric speciation.     

Polygenic inheritance is not necessary for sympatric speciation by sexual selection

 The theoretical possibility of sympatric speciation by sexual selection has been demonstrated by a number of mathematical models. Although these models assumed that sexually selected traits are additively determined by many genes, recent empirical studies suggest that many sexually selected traits are determined by major gene inheritance. Thus, using a mathematical simulation model, this article examines whether sympatric speciation by sexual selection can occur when sexually selected traits are determined by major gene inheritance. The model reveals that speciation can occur with major gene inheritance of sexually selected traits. Simulations show that speciation from an initially monomorphic population occurs via two successive Fisher's runaway processes of sexual selection. The first runaway causes the unidirectional evolution of male secondary sexual character toward one extreme in the trait space and of female mate preference for such a character. The second runaway then drives the male character and female preference of a part of the population toward the other extreme in the trait space, splitting the population into two reproductively isolated subgroups. The current results reinforce the plausibility of sympatric speciation by sexual selection. Received: January 30, 2002 / Accepted: June 27, 2002