what causes the reproductive isolation that can lead to speciation
Abstract
Rates of species formation vary widely beyond the tree of life and contribute to many of the almost hitting large-scale patterns in biological diverseness. For the past few decades, nigh inquiry on speciation has focused on the evolution of barriers to gene flow between populations. The nowadays review discusses the relationship betwixt these barriers, collectively known as 'reproductive isolation', and the rate at which speciation occurs. Although reproductive isolation plays a primal part in the maintenance of biological variety, there is trivial evidence to advise that any forms of reproductive isolation serve as charge per unit-limiting controls on speciation rates as measured over macroevolutionary timescales. Identifying rate-limiting steps of the speciation procedure is critical for understanding why we observe the numbers of species that we do and besides for explaining why some groups of organisms have more species than others. More generally, if reproductive isolation is not the charge per unit-limiting control on speciation rates, then factors other than reproductive isolation must exist involved in speciation and our definition of speciation should be expanded to incorporate these boosted processes.
Introduction
At any given location on Earth, biological multifariousness is packaged into more than-or-less detached units that we typically refer to as 'species'. This fact has been evident to naturalists and philosophers for many centuries and is reflected by the ease with which y'all can use a field guide to identify the birds and trees in your backyard. Science has settled the matter of whether these distinct groups (species, future) exist in a full general sense (Mayr, 1992; Rieseberg, Woods & Baack, 2006), even if the boundaries of any detail species in space and fourth dimension may be unclear. Fifty-fifty Darwin, who was famously skeptical nigh the reality of species as a special category, felt that they represented 'tolerably well-defined objects' (Darwin, 1859).
In the first one-half of the 20th Century, ideas near species and speciation underwent a revolution that shapes much of the prevailing paradigm for understanding the origins of biological variety. This revolution involved a new conceptualization of species, one where species were defined by the processes that kept them apart. These processes, collectively termed 'reproductive isolation', formed the cornerstone of the new 'biological species concept'. The biological species concept (BSC) was popularized by Ernst Mayr (Mayr, 1942, 1963) and generally defines species every bit 'groups of interbreeding natural populations that are reproductively isolated from other such groups' (Mayr, 1970).
Reproductive isolation tin take many forms. Information technology may involve the presence of distinctive morphological, behavioural or other signals that are involved in mate recognition. It may involve ecological factors that affect the fitness of hybrid offspring in nature. For instance, hybrid genotypes may have lower survivorship than pure genotypes of either parental form. Reproductive isolation may involve genetic incompatibilities between species that result in the sterility or inviability of hybrid offspring. There are many potential barriers to gene menstruation, and they have been catalogued at length in recent treatments of speciation (Coyne & Orr, 2004; Price, 2008; Sobel et al., 2010; Nosil, 2012).
The study of speciation has largely been the study of the factors that generate and maintain reproductive isolation (Coyne & Orr, 2004; Wu & Ting, 2004; Mahehwari & Barbash, 2011; Nosil, 2012). In a recent introductory textbook on evolutionary biology (Futuyma, 2009), speciation is defined equally the 'evolution of reproductive isolation within an ancestral species, resulting in two or more descendant species'. This view conspicuously dominates across near of evolutionary biology. In their seminal volume on speciation, Coyne & Orr (2004: 39) observed that 'virtually every recent newspaper on the origin of species, theoretical or experimental, deals with the origin of isolating barriers'. This fact is unsurprising because reproductive isolation must exist the master concern of a speciation prototype that defines the procedure in terms of reproductive isolation itself.
In this review, I argue that a near-exclusive focus on reproductive isolation in speciation research has hindered our ability to explicate large-scale diverseness patterns. It is increasingly axiomatic that the charge per unit at which speciation occurs varies widely across the tree of life ( Smith et al., 2011; Jetz et al., 2012; Beaulieu & Donoghue, 2013; Near et al., 2013; Rabosky et al., 2013), and we know very little about the factors that determine these rates. Many of the nearly striking large-scale patterns in biological diversity are macroevolutionary in nature and can only be answered, at least in part, by agreement the determinants of the rate at which speciation occurs. Why are there so many species of flowering plants? Why are there threescore 000 species of living vertebrates and not 6000 or 600 000? Why are lungfishes and coelacanths and ginkgoes so depauperate in species diversity? Why are at that place so many species in the tropics? Of course, diverseness is a function of both speciation and extinction, and information technology is the relative balance of these processes that determines the dynamics of species richness in time. Although some of the patterns described above may reflect variation in extinction rates (rather than speciation per se), many studies that have explicitly modelled the contribution of speciation charge per unit variation to big scale diversity patterns have institute a compelling indicate of differential speciation on multifariousness patterns ( Rabosky et al., 2013; Belmaker & Jetz, 2015; Rabosky, Title & Huang, 2015).
All of the questions outlined higher up (and many more than) are ultimately questions about which gene or factors are 'rate-limiting controls' on speciation and/or extinction dynamics as measured at macroevolutionary scales. More generally, we cannot assume that the causes of population splitting observed over brusque timescales can be extrapolated to the dynamics of species that play out over vastly longer geological timescales without rigorous tests to support this assumption. I advocate a more inclusive view of speciation that accounts for alternative processes, largely neglected in contemporary speciation research, which may provide the charge per unit-limiting controls on the generation of biological diversity.
Taxonomic Speciation Rates
Most enquiry on the origin of species has focused on reproductive isolation, although a parallel inquiry programme on speciation rates has proceeded without interpreting patterns through the framework of reproductive isolation. This arroyo has its roots in the palaeobiological revolution of the 1970s, in which quantitative models for species formation and extinction were developed to report the appearances and disappearances of individual taxa from the fossil record ( Raup et al., 1973; Stanley, 1975; Sepkoski, 1978; Raup, 1985). The statistical tools developed for studying speciation in the fossil tape (Raup, 1985) take been applied to time-calibrated phylogenetic trees that contain information on living species but (Nee, May & Harvey, 1994; Rabosky & Lovette, 2008; Morlon, Potts & Plotkin, 2010; Etienne & Haegeman, 2012; Pyron & Burbrink, 2013; Stadler, 2013; Moen & Morlon, 2014). These methods have been used to quantify speciation rates in a wide range of taxa, spurred by the rapid increase in the availability of time-calibrated phylogenetic copse based on Dna sequence data.
From a macroevolutionary perspective, the rate of speciation is a statistical description of the per-species charge per unit at which new taxonomic diverseness arises. These rates are referred to hither equally 'taxonomic speciation rates' to reverberate the fact that they are based on species units as recognized by taxonomic do. To be articulate, the reference is to rates of new species origination (i.e. the charge per unit of advent of new species, every bit defined taxonomically) and non net rates of lineage diversification. Internet rates of lineage diversification reflect the balance of species origination and extinction and make up one's mind the dynamics of species richness through time; this is not the aforementioned equally the rate at which diversity arises, which is the focus of the nowadays review. Every bit discussed beneath, these taxonomic speciation rates are not necessarily the same as 'biological speciation rates', defined past Coyne & Orr (2004) as the charge per unit at which reproductively isolated lineages arise. Palaeontological studies demonstrated variation in evolutionary rates amid major groups of organisms (Stanley, 1979; Jablonski, 1986; Sepkoski, 1998), although phylogenetic diversification studies have provided a much higher level of resolution into the dynamics of speciation (but not extinction; Ezard et al., 2011). One of the almost of import results emerging from this research is the extent to which taxonomic speciation rates vary, even between closely-related groups of organisms. Figure 1 shows a pattern of speciation rate variation across a phylogeny of living birds ( Jetz et al., 2012), as inferred using a recently-developed method for quantifying speciation rate heterogeneity (Rabosky, 2014). Across all birds, speciation rates measured over macroevolutionary timescales vary by approximately 3000% ( Rabosky et al., 2015).
Figure ane.
A, per-lineage rates of speciation across a time-calibrated phylogenetic tree of 6670 species of extant birds (67% of the total diversity) as inferred using a statistical model that simultaneously estimates the magnitude of rate variation through time and across lineages. Colours correspond to the instantaneous rate of speciation at each point in the tree. The fastest 5% of rates exceed 0.4 species Myr–1 (dark red). Analysis of evolutionary rates explicitly accounts for extinction, although simply speciation rates are shown. B, estimated present-day speciation rates for all 6670 species; these are simply the all-time guess of the instantaneous rate of speciation for each tip in the phylogeny. Inset images describe representative birds with fast (western gull, Larus occidentalis) and slow (become-away-bird, Corythaixoides leucogaster) rates of speciation. The phylogenetic dataset is from Jetz et al. (2012) and speciation rate assay is described in Rabosky & Matute (2013).
Figure 1.
A, per-lineage rates of speciation beyond a time-calibrated phylogenetic tree of 6670 species of extant birds (67% of the total diverseness) every bit inferred using a statistical model that simultaneously estimates the magnitude of rate variation through time and across lineages. Colours correspond to the instantaneous rate of speciation at each point in the tree. The fastest 5% of rates exceed 0.4 species Myr–1 (dark ruddy). Assay of evolutionary rates explicitly accounts for extinction, although only speciation rates are shown. B, estimated present-day speciation rates for all 6670 species; these are simply the all-time estimate of the instantaneous rate of speciation for each tip in the phylogeny. Inset images describe representative birds with fast (western gull, Larus occidentalis) and tiresome (go-abroad-bird, Corythaixoides leucogaster) rates of speciation. The phylogenetic dataset is from Jetz et al. (2012) and speciation rate analysis is described in Rabosky & Matute (2013).
Interpretation of 'Speciation Rate' Depends on the Significant of Species
Species delimited past the strict application of the biological species concept do not necessarily stand for to the set of species defined past taxonomic practice. Despite the view among many population geneticists that the BSC is mainstream in modern evolutionary biological science, taxonomic exercise largely ignores the BSC and species are by and large defined on the basis of phenotypic distinctiveness (Mallet, 2007), occasionally with supporting evidence from molecular phylogenies or population genetics. Coalescent-based species delimitation using population genetic data ( Pons et al., 2006; Yang & Rannala, 2010) represents a trend towards greater practical awarding of BSC-similar species concepts to taxonomy ( Fujita et al., 2012), although the use of these models is notwithstanding restricted to a small fraction of annual taxonomic volume. Despite the utilize of sophisticated species delimitation approaches in general phylogenetics journals with a broad readership (eastward.g. Systematic Biology; Molecular Phylogenetics and Evolution), the merchandise journals of taxonomy (east.g. Zootaxa), where the vast majority of new species are described, overwhelmingly employ morphological distinctiveness as the primary criterion for species status.
In some groups, there is bear witness that reproductively isolated populations of very recent origin are rarely recognized as distinct (taxonomic) species. For example, autopolyploid lineages in plants are generally not recognized equally distinct from the progenitor species, fifty-fifty when such recognition is potentially warranted nether the BSC ( Soltis et al., 2007). Hundreds, perhaps thousands, of fish lineages in postglacial lakes beyond North America, Eurasia, and Iceland accept diverged into phenotypically and ecologically distinctive forms (Skulason, Noakes & Snorrason, 1989; Bernatchez, Chouinard & Lu, 1999; McKinnon & Rundle, 2002; Hudson et al., 2005), nonetheless these forms are very rarely afforded full species status by taxonomists. Many of these divergent within-lake fish lineages are unlikely to predate the final glacial cycle (approximately 30 000 years BP). Including these forms as total species in macroevolutionary rate analyses would lead to a substantially unlike interpretation of speciation rate (Fig. 2).
Effigy two.
Culling species taxonomies can atomic number 82 to radically different perspectives on species and speciation. A, fourth dimension-calibrated phylogeny for stickleback fishes (Gasterosteidae) from Rabosky et al. (2013). Difference times are broadly congruent with the known fossil history for the genus (Bell, Stewart & Park, 2009). B, hypothetical shape of the stickleback phylogeny if some of the numerous intraspecific morphological variants (open circles) inside the threespine stickleback (Gasterosteus aculeatus) are elevated to full species status. Many freshwater stickleback populations are morphologically distinct from the marine ancestral form and potentially warrant recognition equally distinct biological species (Moodie & Reimchen, 1976; Mcphail, 1994; Bell, 1995; Nelson, 2006; Reimchen et al., 2013); there are potentially dozens or hundreds of such forms. Bong (1995) suggests that, given the extent of morphological parallelism among divergent forms, '… it is neither practical nor useful to depict the biological species inside the Thou. aculeatus complex as separate taxonomic species'. However, given that many such forms could exist recognized as distinct taxonomic species, it is worth considering how their recognition would modify our interpretation of speciation rates. Previous studies on speciation rates across fishes ( Nigh et al., 2013; Rabosky et al., 2013) include but data from deep nodes (dark circles). Notwithstanding, recent divergences, nearly all of which are no older than the almost recent glacial maximum (arrow), are ignored by this arroyo. For the phylogeny in (A), the maximum likelihood estimate of the speciation rate under a constant-rate birth-death model ( Nee et al., 1994) is 0.055 lineages Myr–1. For the phylogeny in (B), which assumes the presence of 30 biological species in 'Gasterosteus aculueatus', all of which take diverged inside the past 30 000 years, we infer a speciation charge per unit of 65.four lineages Myr–i. The number of recently-diverged species spliced into the phylogeny shown in (B) is arbitrary, although it illustrates the profound effects that taxonomic decisions tin can accept on inferences about speciation charge per unit. Understanding the relationship between speciation as studied at population genetic scales (open circles) and macroevolutionary scales (dark circles) is one of the central challenges for the future of speciation research.
Effigy 2.
Alternative species taxonomies can pb to radically dissimilar perspectives on species and speciation. A, fourth dimension-calibrated phylogeny for stickleback fishes (Gasterosteidae) from Rabosky et al. (2013). Divergence times are broadly congruent with the known fossil history for the genus (Bong, Stewart & Park, 2009). B, hypothetical shape of the stickleback phylogeny if some of the numerous intraspecific morphological variants (open up circles) inside the threespine stickleback (Gasterosteus aculeatus) are elevated to full species status. Many freshwater stickleback populations are morphologically singled-out from the marine ancestral form and potentially warrant recognition as distinct biological species (Moodie & Reimchen, 1976; Mcphail, 1994; Bong, 1995; Nelson, 2006; Reimchen et al., 2013); at that place are potentially dozens or hundreds of such forms. Bell (1995) suggests that, given the extent of morphological parallelism amid divergent forms, '… it is neither practical nor useful to describe the biological species within the Yard. aculeatus complex every bit separate taxonomic species'. However, given that many such forms could be recognized as distinct taxonomic species, it is worth considering how their recognition would change our interpretation of speciation rates. Previous studies on speciation rates across fishes ( Near et al., 2013; Rabosky et al., 2013) include just information from deep nodes (dark circles). However, recent divergences, almost all of which are no older than the most recent glacial maximum (arrow), are ignored past this approach. For the phylogeny in (A), the maximum likelihood approximate of the speciation charge per unit nether a constant-rate birth-death model ( Nee et al., 1994) is 0.055 lineages Myr–i. For the phylogeny in (B), which assumes the presence of 30 biological species in 'Gasterosteus aculueatus', all of which have diverged within the past 30 000 years, we infer a speciation rate of 65.iv lineages Myr–1. The number of recently-diverged species spliced into the phylogeny shown in (B) is capricious, although it illustrates the profound effects that taxonomic decisions can have on inferences most speciation rate. Agreement the relationship betwixt speciation as studied at population genetic scales (open circles) and macroevolutionary scales (dark circles) is one of the fundamental challenges for the hereafter of speciation inquiry.
The relationship between species under the BSC and taxonomic practice is complex and will not be reviewed here. However, information technology is important to recognize that speciation rates equally typically inferred from phylogenetic and palaeontological information demand not correspond to those that we would estimate if we were apply to apply the BSC consistently across all lineages inside the same group of organisms. The 'biological speciation charge per unit' every bit described by Coyne & Orr (2004) is, in practice, a taxonomic speciation rate, and it may be singled-out from the rate at which reproductively isolated lineages ascend. Despite the inherent fuzziness of 'species' as used in macroevolutionary studies, they are all that we have to work with until units at the tips of the tree of life are delimited using equivalent criteria. Given the difficulty in identifying a unmarried species concept that works for all groups of organisms (Van Valen, 1976; Harrison, 1998; Mallet, 2007; de Queiroz, 2007), it is unlikely that nosotros will ever achieve such equivalence. My view is that, given the full general reluctance to accredit full species status to very recently diverged forms, the 'taxonomic species concept' that underlies evolutionary rate estimates is biased towards the recognition of deeper lineages and by and large neglects recent divergences that might exist labeled 'incipient species', 'isolates' (Mayr, 1963), 'neospecies' (Levin, 2000) or 'within-species lineages' (Dynesius & Jansson, 2014). As such, 'speciation rates' as estimated from established taxonomies will generally describe lineage dynamics at a phylogenetic scale that ignores the charge per unit at which incipient species are generated.
What Controls the Rate of Speciation?
Reproductive isolation is clearly an important component of the speciation process and is disquisitional for the maintenance of diverseness. In the absence of reproductive isolation, interbreeding between (sexual) species should result in the collapse of taxonomic diverseness. This phenomenon is clearly not what we observe: many species are able to coexist in the same location at the aforementioned time as maintaining their distinctiveness. Nonetheless, other factors tin influence taxonomic speciation rates all the same are distinct from reproductive isolation (Allmon, 1992; Levin, 2000; Rosenblum et al., 2012). Ernst Mayr, an builder of the biological species concept, provided one of the clearest statements of major factors that decide speciation rates. In Animal Species and Evolution (1963), Mayr notes that the rate of speciation depends on:
'… (1) the frequency of barriers, that is, of factors producing geographical isolates, (2) the rates at which geographical isolates become genetically transformed and more specifically at which they acquire isolating mechanisms, and (iii) the degree of ecological diversity offer vacant ecological niches to newly arising species' (Mayr, 1963: 575).
Among these three categories, only item (2) would traditionally exist associated with reproductive isolation. Mayr explains that item (3) – ecological niche availability – is important for successful speciation, because the presence of a vacant niche enables incipient species ('isolates') to persist in time. As Mayr stated (Mayr, 1963: 554): 'What does it matter if 98 or 99 percentage among 100 founder populations or other isolates fall past the wayside? All is well and evolutionary progress assured as long as one of them one time in awhile discovers a new niche'. There is an irony to the set of controls listed here because Mayr (along with Theodosius Dobzhansky) is one of the scientists most widely credited for focusing our collective attending on reproductive isolation equally the defining feature of speciation (Coyne & Orr, 2004). More recently, Allmon (1992) and Dynesius & Jansson (2014) reformulated Mayr'southward three controls on speciation, noting that, in some cases, several of these components may collaborate synergistically. Table 1 provides an overview of the full general types of processes that tin influence taxonomic speciation rates.
Table one.
Controls on speciation rates as measured at macroevolutionary scales: examples are speculative simply prove characteristics suggesting the action of the focal control
| Command | Description | Possible examples |
|---|---|---|
| Charge per unit of splitting | The charge per unit at which a single population splits into 2 populations | High rates of long-distance dispersal in Zosterops birds ('white-eyes') leads to the establishment of new populations on remote islands and to rapid speciation rates for the clade as a whole ( Moyle et al., 2009) |
| Reproductive isolation | Evolution of biological traits that reduce gene flow between populations | Reproductive isolation, mediated by mating preferences and male person color phenotypes, evolves quickly between populations of Lake Victoria cichlid fishes ( Seehausen et al., 2008). This group is known to have extremely rapid rates of speciation ( Johnson et al., 1996) |
| Population persistence | Incipient species avoid demographic extinction | Similarity to parental forms may limit persistence of recently-formed polyploid establish species (Levin, 2000; Mayrose et al., 2011; Arrigo & Barker, 2012) |
| Control | Description | Possible examples |
|---|---|---|
| Rate of splitting | The rate at which a single population splits into ii populations | High rates of long-altitude dispersal in Zosterops birds ('white-optics') leads to the institution of new populations on remote islands and to rapid speciation rates for the clade as a whole ( Moyle et al., 2009) |
| Reproductive isolation | Evolution of biological traits that reduce gene menstruum between populations | Reproductive isolation, mediated by mating preferences and male color phenotypes, evolves chop-chop between populations of Lake Victoria cichlid fishes ( Seehausen et al., 2008). This group is known to have extremely rapid rates of speciation ( Johnson et al., 1996) |
| Population persistence | Incipient species avoid demographic extinction | Similarity to parental forms may limit persistence of recently-formed polyploid found species (Levin, 2000; Mayrose et al., 2011; Arrigo & Barker, 2012) |
Tabular array 1.
Controls on speciation rates as measured at macroevolutionary scales: examples are speculative but bear witness characteristics suggesting the activity of the focal control
| Control | Clarification | Possible examples |
|---|---|---|
| Charge per unit of splitting | The rate at which a single population splits into 2 populations | High rates of long-altitude dispersal in Zosterops birds ('white-eyes') leads to the establishment of new populations on remote islands and to rapid speciation rates for the clade as a whole ( Moyle et al., 2009) |
| Reproductive isolation | Evolution of biological traits that reduce gene menstruum between populations | Reproductive isolation, mediated by mating preferences and male color phenotypes, evolves quickly between populations of Lake Victoria cichlid fishes ( Seehausen et al., 2008). This group is known to take extremely rapid rates of speciation ( Johnson et al., 1996) |
| Population persistence | Incipient species avert demographic extinction | Similarity to parental forms may limit persistence of recently-formed polyploid establish species (Levin, 2000; Mayrose et al., 2011; Arrigo & Barker, 2012) |
| Control | Description | Possible examples |
|---|---|---|
| Charge per unit of splitting | The charge per unit at which a single population splits into two populations | Loftier rates of long-distance dispersal in Zosterops birds ('white-eyes') leads to the establishment of new populations on remote islands and to rapid speciation rates for the clade as a whole ( Moyle et al., 2009) |
| Reproductive isolation | Development of biological traits that reduce gene flow between populations | Reproductive isolation, mediated by mating preferences and male colour phenotypes, evolves rapidly betwixt populations of Lake Victoria cichlid fishes ( Seehausen et al., 2008). This group is known to take extremely rapid rates of speciation ( Johnson et al., 1996) |
| Population persistence | Incipient species avoid demographic extinction | Similarity to parental forms may limit persistence of recently-formed polyploid constitute species (Levin, 2000; Mayrose et al., 2011; Arrigo & Barker, 2012) |
As discussed higher up, diversification charge per unit is the difference between per-taxon speciation and extinction rates and determines the expected diversity of a clade through time. The semantics of extinction cannot be ignored considering ane of the major controls on speciation identified (Mayr, 1963; Allmon, 1992; Stanley, 2008; Rosenblum et al., 2012) involves the persistence (e.yard. 'non-extinction') of isolated populations or incipient species through time (Table 1). The boundary between speciation and extinction may be much blurrier than nosotros typically acknowledge. At the macroevolutionary scale, 'extinction' is applied to taxa that are diagnosable in the fossil record and that have had a history of existence as independent evolutionary lineages.
A failure of incipient forms to persist is conceptually distinct from extinction equally typically understood because it involves populations that have had only the briefest beingness every bit independent lineages. The persistence control can apply to lineages that are geographically isolated but that show no reproductive isolation and no diagnostic phenotypic traits relative to a parental population. It is inappropriate to presume equivalence between extinction at the macroevolutionary calibration (eastward.thou. the loss of a species) and extinction of potentially localized populations, which might only represent demographic loss within a single undifferentiated species. Moreover, the failure of recently-isolated populations to persist, whether they are reproductively isolated or not, is largely invisible in the fossil record (Rabosky, 2013). Equally such, there is (in general) no observable extinction associated with the failure of incipient forms to persist.
Our full general binary distinction between speciation and extinction thus leads to terminological defoliation when discussing these processes. From the macroevolutionary perspective adopted in the preseent review, I concord with Mayr'southward view that 'persistence of incipient species' is a part of the concept of speciation and separate from the processes by which established lineages become extinct. This distinction follows naturally from a conceptualization of species origination that tin be measured over palaeontological or phylogenetic scales. Moreover, treating persistence equally part of speciation is warranted on strictly pragmatic grounds if we are to continue studying speciation rates using time-calibrated phylogenies of extant taxa and the fossil record. Disallowment a radical change in taxonomic do, speciation rates as measured at a macroevolutionary scale (and equally published in hundreds of recent journal articles) are an consequence of the three controls discussed above. Hence, even formal models that can distinguish between speciation and extinction rates on phylogenetic trees (Maddison, Midford & Otto, 2007; FitzJohn, Maddison & Otto, 2009; Goldberg, Lancaster & Ree, 2011) are unable to divide the effects of lineage persistence from other factors that influence speciation rate (but, for a useful analytical arroyo to this trouble, see Etienne, Morlon & Lambert, 2014). Yet, ultimately, it will be most fruitful if we motility across a dichotomous view of speciation and extinction as the fundamental processes of lineage diversification (as many researchers cited in the present review have already done).
Successful speciation thus entails the splitting of populations, the development of biologically-based barriers to factor flow (reproductive isolation), and the persistence of incipient species. All of these general factors might exist involved in the speciation process, although information technology is the rate-limiting factor lone, which could be any of the three, that determines the taxonomic speciation rate. This rate, together with the rate at which established lineages get extinct, is the virtually important with respect to explaining why the 'quantity' of biological diverseness is what nosotros observe it to be. These factors are not mutually exclusive. For instance, divergent natural selection that favours multiple phenotypes inside a species can simultaneously promote population splitting and reproductive isolation, every bit in models where speciation occurs in the presence of substantial factor flow ( Gagnaire et al., 2013; Martin et al., 2013). Anecdotally, it is clear that reproductive isolation can evolve rapidly in some taxa that accept slow rates of speciation every bit measured at macroevolutionary timescales (Rabosky, 2013). Stickleback fishes can evolve reproductive isolation quite rapidly and take formed morphologically distinctive populations or even pairs of incipient species in many postglacial lakes (Schluter, 1996; Rundle et al., 2000; Reimchen, Bergstrom & Nosil, 2013). These differences have potentially evolved subsequent to the Last Glacial Maximum (< 30 000 years BP). However, incipient stickleback forms only rarely become taxonomically distinct species considering they fail to persist through deep fourth dimension (McKinnon & Rundle, 2002). McPhail (1994) discussed the paradox between the depression species richness of stickleback fishes in general (Fig. 2) and their propensity for rapid speciation in the present day: '… most divergent [stickleback] populations and biological species that evolve under these atmospheric condition are doomed either to genetic swamping or to extinction. They flourish briefly and then disappear without appreciable bear on on the evolutionary trajectory of the main body of the species' (McPhail, 1994: 437). Hence, reproductive isolation does non appear to be a rate-limiting control on stickleback speciation rates every bit measured over macroevolutionary timescales.
The state of affairs in nature is rather more complex than that suggested by the outline in a higher place because reproductive isolation is often incomplete and, at least in some taxa, has been shown to break down in ecological time (Seehausen, van Alphen & Witte, 1997; Nosil, Harmon & Seehausen, 2009). For case, in North America's Great Lakes, an owned species flock of Coregonus whitefishes appears to have undergone 'speciation in opposite' in historical times. Most forms appear to have disappeared as a result of hybridization (Todd & Stedman, 1989), and like merging of incipient or recently diverged forms has occurred in stickleback fishes (Gow, Peichel & Taylor, 2006; Taylor et al., 2006) and Lake Victoria cichlids ( Seehausen et al., 1997). Darwin'south finches are some other instance of a group where reproductive isolation betwixt morphological forms appears to lack temporal stability (Grant & Grant, 1997), leading to widespread genetic homogenization among morphological forms inhabiting the same island ( Farrington et al., 2014; McKay & Zink, 2015). It would be premature, notwithstanding, to conclude that the limiting step on taxonomic speciation rates in these and other taxa is a function of the robustness of reproductive isolation and non of other potential controls.
Many studies have addressed the relationships between specific organismal traits and speciation rates on phylogenetic trees. This literature is non reviewed hither, in office because the mechanisms by which traits influence speciation are rarely known or straight tested. For example, an clan between a key ecological trait and speciation rate could arise if the trait accelerates the evolution of reproductive isolation in lineages where it is present. However, it is also possible that the trait influences the speciation rate through its furnishings on population persistence or institution. Thus, the connection between traits and speciation mostly relies on assumptions about the relevance of the trait for the controls described above. An culling approach that more than directly connects specific components of reproductive isolation to taxonomic speciation rates is discussed beneath. Nonetheless, a number of researchers have considered the furnishings of dispersal and geographical range dynamics for speciation charge per unit (Sol, Stirling & Lefebvre, 2005; Weeks & Claramunt, 2014); these processes presumably influence speciation not through their furnishings on reproductive isolation, but through the institution of new populations (Cost, 2010) and/or by facilitating population persistence (Harnik, Simpson & Payne, 2012). Price et al. (2014) suggested that speciation rates in Himalayan passerine birds were influenced more by ecological controls on range expansions than past the build up of reproductive isolation. An interesting twist on the speciation controls listed above is that incomplete reproductive isolation may itself limit range expansion (Weir & Price, 2011), thus indirectly facilitating population persistence (through larger geographical range), too every bit the establishment of new populations for subsequent speciation. This idea remains to be tested but would support the possibility that reproductive isolation and other controls may interact to jointly influence the charge per unit of speciation.
Information technology is generally accepted that some forms of reproductive isolation might have little relevance to the speciation process. For example, intrinsic postzygotic isolation (i.e. genetic incompatibilities between species that crusade hybrid dysfunction) might arise long after successful speciation has occurred (Grant & Grant, 1997; Coyne & Orr, 2004; Bolnick & Near, 2005; Wiens, Engstrom & Chippindale, 2006), implying that these forms of reproductive isolation contribute little to the speciation process. However, there is no evidence available indicating that whatever forms of reproductive isolation serve every bit rate-limiting controls on taxonomic speciation rates. To be articulate, in that location is little evidence to suggest that whatever other controls (Table i) are generally more important than reproductive isolation at this scale, although few studies have yet assessed the relative contributions of these factors to variation in speciation charge per unit. Identifying these controls and clarifying their genetic, demographic, and ecological mechanisms is one of the greatest challenges for evolutionary biology in the coming years.
Testing the Role of Reproductive Isolation in Speciation Dynamics
Because reproductive isolation tin can be quantified, it is possible to directly exam whether it is a charge per unit-limiting control on taxonomic speciation rates (Rabosky & Matute, 2013). All else being equal, lineages that evolve reproductive isolation more than quickly should be characterized past faster rates of speciation. As a thought experiment, consider 2 singled-out species, X and Y, such that Ten belongs to a clade of organisms that can evolve reproductive isolation chop-chop, and Y belongs to a clade where reproductive isolation evolves slowly. Suppose that a geological event splits both species Ten and Y into two populations: X ane and X 2, and Y 1 and Y 2. After an equivalent corporeality of time has elapsed, populations 10 ane and 10 ii would show greater reproductive isolation than populations Y ane and Y 2. If the rate at which reproductive isolation evolves is the charge per unit-limiting control on speciation rates, then the lineage to which species 10 belongs should, over long timescales, speciate more rapidly than the lineage of Y. If another factor is the rate-limiting control on speciation rates, and then the realized charge per unit of speciation will be independent of the rate at which reproductive isolation evolves.
This logic forms the basis of a statistical test for the contribution of any form of reproductive isolation to macroevolutionary speciation rates. Ane tin quantify the rate at which particular components of reproductive isolation evolve in different clades or lineages (Fig. 3) and test whether variation in the rate of development of reproductive isolation predicts speciation rates. Possible relationships between these quantities are shown in Effigy 4. The key advantage of this approach is that information technology avoids assumptions most the presumed effects of particular organismal traits on the evolution of reproductive isolation (Coyne & Orr, 2004) and estimates parameters of the process direct. This test has been applied to birds and to drosophilid flies aiming to test whether the charge per unit at which lineages acquire postzygotic genetic incompatibilities (due east.chiliad. alleles that crusade interspecies hybrids to be sterile or inviable) is associated with speciation rates. Although individual clades of both birds and flies varied with respect to the rate at which they evolved at least 1 component of reproductive isolation, this variation was unrelated to taxonomic speciation rates (Rabosky & Matute, 2013). Yet, the results reported by Rabosky & Matute (2013) should be interpreted with circumspection, given uncertainties in quantifying speciation charge per unit variation and the rate at which reproductive isolation evolves. For example, the biology of intrinsic reproductive isolation in drosophilid flies has been studied by dozens of researchers over much of the past century, generating peradventure the highest-resolution dataset on reproductive isolation for whatever group of organisms (Yukilevich, 2012). However, our understanding of taxonomic speciation rates in the drosophilidae is poor: indeed, it is possible that hundreds or thousands of singled-out drosophilid taxa remain to be described (Markow & O'Grady, 2006). Such taxonomic inadequacy has implications for the speciation rates used past Rabosky & Matute (2013). Similarly, our analyses of avian postzygotic isolation were largely based on a single compilation of avian hybrids (Gray, 1958) and we had no straight data on premating isolation for birds.
Effigy three.
Pairwise postzygotic isolation from interspecific crosses of birds as a office of the pairwise genetic altitude between them. Results are shown for ii major clades (pheasants, Phasianidae; parrots, Psittacidae). For a given level of genetic deviation, pheasants testify greater levels of postzygotic isolation than the parrots, indicating that this sort of reproductive isolation accumulates more quickly in pheasants than in parrots. If intrinsic postzygotic isolation (hybrid inviability and sterility) is the dominant control on speciation rates, pheasants should have faster rates of speciation than parrots. Note that relationships are bounded at 0 (all hybrid offspring fully feasible and fertile) and 1 (no offspring produced, or all offspring sterile). Lines evidence fitted linear relationships between reproductive isolation and genetic distance for each clade. Data are from Price & Bouvier (2002) and Gray (1958); analyses are from Rabosky and Matute (2013). For this pair of clades, speciation rates are faster in the clade with faster rates of development of reproductive isolation (pheasants: speciation = 0.26 lineages Myr–1; parrots: speciation = 0.22 lineages Myr–ane). However, beyond all birds, these quantities appear to be unrelated.
Figure 3.
Pairwise postzygotic isolation from interspecific crosses of birds as a function of the pairwise genetic distance between them. Results are shown for ii major clades (pheasants, Phasianidae; parrots, Psittacidae). For a given level of genetic divergence, pheasants testify greater levels of postzygotic isolation than the parrots, indicating that this sort of reproductive isolation accumulates more quickly in pheasants than in parrots. If intrinsic postzygotic isolation (hybrid inviability and sterility) is the dominant control on speciation rates, pheasants should have faster rates of speciation than parrots. Note that relationships are divisional at 0 (all hybrid offspring fully feasible and fertile) and 1 (no offspring produced, or all offspring sterile). Lines evidence fitted linear relationships between reproductive isolation and genetic altitude for each clade. Data are from Cost & Bouvier (2002) and Gray (1958); analyses are from Rabosky and Matute (2013). For this pair of clades, speciation rates are faster in the clade with faster rates of development of reproductive isolation (pheasants: speciation = 0.26 lineages Myr–1; parrots: speciation = 0.22 lineages Myr–1). However, beyond all birds, these quantities appear to be unrelated.
Effigy 4.
Some possible relationships between the rate at which lineages evolve reproductive isolation and their rate of speciation. A, directly correspondence, where the evolution of reproductive evolution shows a 1-to-one relationship with the macroevolutionary rate of speciation. In this scenario, the evolution of reproductive isolation is the sectional determinant of macroevolutionary speciation dynamics. B, offset/dampened human relationship, where the charge per unit of evolution of reproductive isolation is the ascendant control on speciation rates, although speciation rates are lower than predicted by the rate of development of reproductive isolation alone. This relationship implies that many populations evolving reproductive isolation fail to persist through deep fourth dimension. C, decoupled, such that reproductive isolation shows no predictive human relationship with macroevolutionary speciation rates. This scenario suggests that reproductive isolation is not the rate-limiting control on the rate of speciation. Adjusted from Rabosky (2013).
Figure 4.
Some possible relationships between the rate at which lineages evolve reproductive isolation and their rate of speciation. A, straight correspondence, where the evolution of reproductive evolution shows a one-to-ane relationship with the macroevolutionary rate of speciation. In this scenario, the evolution of reproductive isolation is the sectional determinant of macroevolutionary speciation dynamics. B, offset/dampened relationship, where the rate of evolution of reproductive isolation is the dominant control on speciation rates, although speciation rates are lower than predicted past the charge per unit of evolution of reproductive isolation alone. This relationship implies that many populations evolving reproductive isolation neglect to persist through deep fourth dimension. C, decoupled, such that reproductive isolation shows no predictive relationship with macroevolutionary speciation rates. This scenario suggests that reproductive isolation is not the rate-limiting control on the rate of speciation. Adapted from Rabosky (2013).
Coyne & Orr (2004) distinguished between two temporal aspects of the speciation procedure: the 'biological speciation interval' (BSI), or the waiting time between the origin of new reproductively isolated lineages, and the 'transition time for biological speciation', or the amount of time required for stiff reproductive isolation to evolve in one case the evolution of isolation has begun. The biological speciation charge per unit is merely the inverse of the biological speciation interval (1/BSI). Coyne & Orr (2004) suggested that there is little reason to wait equivalence betwixt transition times and biological speciation intervals. However, the charge per unit at which reproductive isolation evolves can still be the rate-limiting step on speciation rates even if transition times are much shorter (or longer) than BSIs. For example, the occurrence of fractional intrinsic postzygotic isolation betwixt populations might trigger reinforcement, such that complete prezygotic isolation evolves rapidly in response to maladaptive hybridization (Servedio & Noor, 2003; Matute, 2010). Equally such, the charge per unit-limiting step on taxonomic speciation rates tin notwithstanding exist the charge per unit at which the initial postzygotic isolation arises, even if it is the subsequent development of premating isolation that ultimately drives speciation to completion. This process would potentially be testable past developing more than sophisticated modelling frameworks that enable researchers to distinguish between lineage-specific differences in the charge per unit at which any measurable reproductive isolation arises (eastward.g. duration of the lag stage; Mendelson, Inouye & Rausher, 2004) from the rate at which strong reproductive isolation arises.
A desirable characteristic of the approach illustrated in Figure four is that it provides a fairly direct test of the contribution of reproductive isolation to taxonomic speciation charge per unit. As such, the approach can exist assorted with phylogenetic comparative methods for identifying correlations between specific organismal traits and diversification rates. Numerous studies have establish at to the lowest degree some association between traits and diversification rates (Coyne & Orr, 2004; Jablonski, 2008; Ng & Smith, 2014). Such associations can arise if the traits under consideration increase the rate at which reproductive isolation evolves ( Panhuis et al., 2001; Coyne & Orr, 2004), to which we might add: 'provided that the rate of evolution of reproductive isolation is the rate limiting pace on taxonomic speciation rates'. Still, demonstration that a particular trait is correlated with taxonomic speciation rate does non necessarily imply that the underlying mechanism involves the effects of the trait on reproductive isolation, fifty-fifty if we assume that the trait influences reproductive isolation. Because of the complex means in which traits can influence metapopulation dynamics (Levin, 2000), we should be cautious in bold that whatever particular traits (e.g. sexual dichromatism in animals, floral characteristics, etc.) influence species richness through their effects on reproductive isolation.
It is also important to recognize the limitations of the approach illustrated in Effigy iv. The lack of a relationship between a particular command (east.yard. intrinsic postzygotic reproductive isolation) and speciation rates should not be interpreted as evidence that the control is irrelevant to speciation. It simply means that the control does not determine the rate at which speciation occurs; the command may nonetheless be an integral office of the speciation procedure. Furthermore, observing that one component of reproductive isolation fails to predict speciation rates provides no information about the importance of other forms of reproductive isolation for speciation rates. Finally, the quality of the bachelor phylogenetic, taxonomic, and reproductive isolation data limit the apply of this framework in practice.
Other conceptual tools may provide insight into the function of splitting and persistence controls on speciation rates. The protracted speciation model (Etienne & Rosindell, 2012) is an important theoretical framework for understanding how the origination, extinction, and persistence of incipient species influence the shapes of phylogenetic trees. Recently, Etienne et al. (2014) developed a class of the protracted speciation model that could be fitted to phylogenetic datasets, potentially enabling researchers to estimate parameters associated with both the charge per unit of incipient species formation and the time required for successful speciation. Conceivably, extensions of this general framework may be developed into a formal exam of the relative importance of these and other controls on taxonomic speciation rates.
Conclusions
I suggest that any full general theory of speciation that purports to explain large-scale patterns of biological diversity must be able to explain taxonomic speciation rates as measured using phylogenetic or palaeontological information. The present review has outlined a general framework that can be used to examination whether various components of reproductive isolation serve as rate-limiting steps on the generation of biological variety. Although I have summarized some classic and recent work on speciation charge per unit controls (Mayr, 1963; Allmon, 1992; Rosenblum et al., 2012; Dynesius & Jansson, 2014), my focus in this review has been on the relationship between reproductive isolation and taxonomic speciation rates.
A number of complex issues remain to be resolved, such as the human relationship between taxonomic speciation rates and biological speciation rates. Many researchers accept previously noted the consequences of species delimitation for the report of speciation (Harrison, 1998; Wiens, 2004) and I believe that progress towards understanding speciation ultimately depends on agreement the significant of the taxonomic units on which we base our speciation charge per unit estimates. Concerns near the meaning of species may be even more acute for the fossil tape because fossil species typically stand for stratigraphically distinct morphotypes (Allmon, 2013). With the possible exception of large vertebrates (Roth, 1992), the connection betwixt these forms and nowadays-twenty-four hour period (neontological) species remains poorly known.
During the past few decades, we have learned a nifty deal virtually the processes that maintain the persistence and distinctiveness of species in sympatry. We understand much about the genetic basis for reproductive isolation, which plays a critical role in maintaining species diversity. However, until we understand the relative contribution of reproductive isolation (and other factors) (Table 1) to taxonomic speciation rates, we cannot claim to take answered the most basic questions well-nigh the variety of life that surrounds usa. Today, more than 150 years later the publication of the Origin of Species, I believe that we understand rather less than we typically remember about the processes that created Darwin'southward Entangled Banking concern, 'clothed with many plants of many dissimilar kinds, with birds singing on the bushes, with various insects flitting about, and with worms crawling through the damp world' (Darwin, 1859: 489). However, there is no better fourth dimension than the nowadays to apply the set of methodological and theoretical tools currently at our disposal to the total spectrum of speciation charge per unit controls.
Acknowledgements
I thank Michael E. Alfaro, Alison Davis Rabosky, Richard G. Harrison, Daniel Matute, Amy R. McCune, Trevor Price, Dolph Schluter, Peter Wagner, and several bearding reviewers for their comments on the manuscript and/or discussion of the ideas included herein. This paper was a contribution to a Linnean Society symposium on "Radiation and Extinction: Investigating Clade Dynamics in Deep Time" held on November 10–11, 2014 at the Linnean Society of London and Majestic College London and organised by Anjali Goswami, Philip D. Mannion, and Michael J. Benton, the proceedings of which accept been collated every bit a Special Upshot of the Periodical.
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