A comparative analysis of the mechanisms underlying speciation on Lord Howe Island

On Lord Howe Island, speciation is thought to have taken place in situ in a diverse array of distantly related plant taxa (Metrosideros, Howea and Coprosma; Proc. Natl Acad. Sci. USA 108 , 2011, 13188). We now investigate whether the speciation processes were driven by divergent natural selection in each genus by examining the extent of ecological and genetic divergence. We present new and extensive, ecological and genetic data for all three genera. Consistent with ecologically driven speciation, outlier loci were detected using genome scan methods. This mechanism is supported by individual‐based analyses of genotype–environment correlations within species, demonstrating that local adaptation is currently widespread on the island. Genetic analyses show that prezygotic isolating barriers within species are currently insufficiently strong to allow further population differentiation. Interspecific hybridization was found in both Howea and Coprosma, and species distribution modelling indicates that competitive exclusion may result in selection against admixed individuals. Colonization of new niches, partly fuelled by the rapid generation of new adaptive genotypes via hybridization, appears to have resulted in the adaptive radiation in Coprosma – supporting the ‘Syngameon hypothesis’.     

Phylogenetic Cascades and the Origins of Tropical Diversity

For organisms involved in specialized ecological interactions, the potential exists to have congruent evolutionary histories, such that diversification within one lineage of organisms parallels diversification within another. This model of shared evolutionary history has most often been explored in a bitrophic context, particularly with plants and specialized herbivorous insects, though also with other ecological partners such as vertebrate hosts and their invertebrate parasites. Recently, the possibility has been raised that evolutionary histories might be shared across more than two trophic levels, a phenomenon that we term a phylogenetic cascade. We review previous work on tritrophic diversification and discuss outstanding questions, with an emphasis on plants, caterpillars, and parasitoids, in diverse tropical communities.     

Reproductive isolation among allopatric Drosophila montana populations

An outstanding goal in speciation research is to trace the mode and tempo of the evolution of barriers to gene flow. Such research benefits from studying incipient speciation, in which speciation between populations has not yet occurred, but where multiple potential mechanisms of reproductive isolation (RI: i.e., premating, postmating‐prezygotic (PMPZ), and postzygotic barriers) may act. We used such a system to investigate these barriers among allopatric populations of Drosophila montana. In all heteropopulation crosses we found premating (sexual) isolation, which was either symmetric or asymmetric depending on the population pair compared. Postmating isolation was particularly strong in crosses involving males from one of the study populations, and while sperm were successfully transferred, stored, and motile, we experimentally demonstrated that the majority of eggs produced were unfertilized. Thus, we identified the nature of a PMPZ incompatibility. There was no evidence of intrinsic postzygotic effects. Measures of absolute and relative strengths of pre‐ and postmating barriers showed that populations differed in the mode and magnitude of RI barriers. Our results indicate that incipient RI among populations can be driven by different contributions of both premating and PMPZ barriers occurring between different population pairs and without the evolution of postzygotic barriers.     

You stay,but I Hop: Host shifting near and far co‐dominated the evolution of Enchenopa treehoppers

The importance and prevalence of phylogenetic tracking between hosts and dependent organisms caused by co‐evolution and shifting between closely related host species have been debated for decades. Most studies of phylogenetic tracking among phytophagous insects and their host plants have been limited to insects feeding on a narrow range of host species. However, narrow host ranges can confound phylogenetic tracking (phylogenetic tracking hypothesis) with host shifting between hosts of intermediate relationship (intermediate hypothesis). Here, we investigated the evolutionary history of the Enchenopa binotata complex of treehoppers. Each species in this complex has high host fidelity, but the entire complex uses hosts across eight plant orders. The phylogenies of E. binotata were reconstructed to evaluate whether (1) tracking host phylogeny; or (2) shifting between intermediately related host plants better explains the evolutionary history of E. binotata. Our results suggest that E. binotata primarily shifted between both distant and intermediate host plants regardless of host phylogeny and less frequently tracked the phylogeny of their hosts. These findings indicate that phytophagous insects with high host fidelity, such as E. binotata, are capable of adaptation not only to closely related host plants but also to novel hosts, likely with diverse phenology and defense mechanisms.     

Experimental evidence of genome‐wide impact of ecological selection during early stages of speciation‐with‐gene‐flow

Theory predicts that speciation‐with‐gene‐flow is more likely when the consequences of selection for population divergence transitions from mainly direct effects of selection acting on individual genes to a collective property of all selected genes in the genome. Thus, understanding the direct impacts of ecologically based selection, as well as the indirect effects due to correlations among loci, is critical to understanding speciation. Here, we measure the genome‐wide impacts of host‐associated selection between hawthorn and apple host races of Rhagoletis pomonella (Diptera: Tephritidae), a model for contemporary speciation‐with‐gene‐flow. Allele frequency shifts of 32 455 SNPs induced in a selection experiment based on host phenology were genome wide and highly concordant with genetic divergence between co‐occurring apple and hawthorn flies in nature. This striking genome‐wide similarity between experimental and natural populations of R. pomonella underscores the importance of ecological selection at early stages of divergence and calls for further integration of studies of eco‐evolutionary dynamics and genome divergence.     

Laboratory environments are not conducive for allopatric speciation

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

Existence of a pattern of reproductive character displacement in Homobasidiomycota but not in Ascomycota

Generally, stronger reproductive isolation is expected between sympatric than between allopatric sibling species. Such reproductive character displacement should predominantly affect premating reproductive isolation and can be due to several mechanisms, including population extinction, fusion of insufficiently isolated incipient species and reinforcement of reproductive isolation in response to low hybrid fitness. Experimental data on several taxa have confirmed these theoretical expectations on reproductive character displacement, but they are restricted to animals and a few plants. Using results reported in the literature on crossing experiments in fungi, we compared the degree and the nature of reproductive isolation between allopatric and sympatric species pairs. In accordance with theoretical expectations, we found a pattern of enhanced premating isolation among sympatric sibling species in Homobasidiomycota. By contrast, we did not find evidence for reproductive character displacement in Ascomycota at similar genetic distances. Both allopatric and sympatric species of Ascomycota had similarly low levels of reproductive isolation, being mostly post-zygotic. This suggests that some phylogeny-dependent life-history trait may strongly influence the evolution of reproductive isolation between closely related species. A significant correlation was found between degree of reproductive isolation and genetic divergence among allopatric species of Homobasidiomycota, but not among sympatric ones or among Ascomycota species.     

Morphological divergence and the Quaternary speciation of Actaea purpurea (Ranunculaceae) and its relatives

To understand the process and mechanism of speciation, a detailed analysis of origin and demographic history of recently diverged species pairs is necessary. Here, we investigate the evolutionary history of Actaea purpurea (P.K. Hsiao) J. Compton and its closest relatives, A. japonica Thunb. and A. biternata (Siebold and Zuccarini) Prantl. We aim to estimate important parameters of the divergence event, and to lay the foundation for further investigation of the speciation mechanism of this system. Floral and vegetative traits were measured and analyzed. Genetic structure, divergence history, and historical gene flow were also inferred from the plastid and single nucleotide polymorphism data. Floral traits were divergent, and a strong match between pollinator and floral traits was revealed. Genetically the two species were also well diverged, and the time of divergence was dated to the Pleistocene. The demographic modelling results suggest that A. purpurea had continuous limited gene flow with A. japonica and A. biternata since divergence. More work is now needed to confirm that floral trait divergence was selected by pollinators, as well as to understand how pollinator isolation acts in conjunction with other reproductive barriers to reduce gene flow between the two species.     

Loss-of-imprinting of Peg1 in mouse interspecies hybrids is correlated with altered growth

Previous studies have shown that loss-of-imprinting (LOI) is a regular occurrence in interspecies hybrids of the genus Peromyscus. Furthermore, evidence was presented that indicated that LOI is involved in a placental hybrid dysgenesis effect resulting in abnormal placental growth and thus possibly in speciation. We show here that LOI of the strictly paternally expressed gene Peg1 (also called Mest) occurs in F1 hybrids between Mus musculus (MMU) and M. spretus (MSP). Peg1 LOI is correlated with increased body weight and increased weight of two of the organs tested, kidney and spleen. X-gal staining of tissues derived from Peg1(+/-) x MSP F1 mice, carrying a maternal LacZ knock-in allele of Peg1, demonstrates that LOI is stochastic in that it affects different tissues to variable extents and that, even within one tissue, not all cells are similarly affected. Furthermore, this expression from the maternal allele does not necessarily follow the endogenous paternal Peg1 expression pattern. Our results indicate that LOI occurs in interspecies hybrids in the genus Mus and that altered growth is a frequent outcome of LOI.     

The tempo of trait divergence in geographic isolation: Avian speciation across the Marañon Valley of Peru

Geographic isolation is considered essential to most speciation events, but our understanding of what controls the pace and degree of phenotypic divergence among allopatric populations remains poor. Why do some taxa exhibit phenotypic differentiation across barriers to dispersal, whereas others do not? To test factors controlling phenotypic divergence in allopatry, we employed a comparative phylogeographic approach consisting of replicates of ecologically similar Andean bird species isolated across a major biogeographic barrier, the Marañon Valley of Peru. Our study design leverages variation among codistributed taxa in their degree of plumage, morphometric, and vocal differentiation across the Marañon to examine the tempo of phenotypic evolution. We found that substantial plumage differences between populations required roughly two million years to evolve. In contrast, morphometric trait evolution showed greater idiosyncrasy and stasis. Our results demonstrate that despite a large degree of idiosyncrasy in the relationship between genetic and phenotypic divergence across taxa and environments, comparative studies within regions may reveal predictability in the pace of phenotypic divergence. Our results also suggest that social selection is important for driving differentiation of populations found in similar environments.     

A captive breeding experiment reveals no evidence of reproductive isolation among lineages of a polytypic poison frog

Reproductive isolation is central to the generation of biodiversity, yet a clear understanding of the contributions of alternative reproductive barriers to this process remains elusive. Studies of young lineages that have diverged in ecologically important traits can offer insights into the chronology and relative importance of various isolating mechanisms during speciation. In poison frogs (Dendrobatidae), within‐species lineages often differ dramatically in coloration, a trait subject to natural and sexual selection. Coloration in the strawberry poison frog (Oophaga pumilio) is particularly diverse and previous work suggests the potential for reproductive isolation. We used a captive breeding experiment to assess the extent of reproductive isolation among three allopatric, genetically distinct O. pumilio lineages that differ in coloration. We compared reproduction of within‐ and between‐lineage pairs, predicting that if lineages are isolated, within‐lineage pairs would be most successful. We also examined the fertility and productivity of F1 backcrosses of admixed offspring. We found no evidence suggesting behavioural pre‐zygotic or post‐zygotic reproductive isolation, indicating that isolation would not be maintained by intrinsic mechanisms in the event of secondary contact. Future work should address costs of between‐lineage matings exerted by extrinsic natural and/or sexual selection against admixed offspring.     

Divergence and isolation of cryptic sympatric taxa within the annual legume Amphicarpaea bracteata

The amphicarpic annual legume Amphicarpaea bracteata is unusual in producing aerial and subterranean cleistogamous flowers that always self‐fertilize and, less commonly, aerial chasmogamous flowers that outcross. Although both morphologic and genetic variants are known in this highly selfing species, debate continues over whether this variation is continuous, reflecting the segregation of standing genetic variation, or discontinuous, reflecting distinct taxa that rarely intercross. We characterized SNP variation in 128 individuals in southern Wisconsin to assess within‐ and among‐population variation at 3928 SNPs. We also assessed genotype and leaf morphology in an additional 76 individuals to connect phenotypic variation with genetic variation. Genetic variation maps onto three strongly divergent and highly inbred genetic groups showing little relation to site location. Each group has a distinct phenotype, but the divergence of these groups differs from the varietal divisions previously identified based on morphological characters. Like previous authors, we argue that the taxonomy of this species should be revised. Despite extensive sympatry, estimates of among‐group migration rates are low, and hybrid individuals were at low frequency (<2%) in our dataset. Restricted gene flow likely results from high selfing rates and partial reproductive incompatibility as evidenced by the U‐shaped distribution of pairwise F_ST values reflecting “islands” of genomic divergence. These islands may be associated with hybrid incompatibility loci that arose in allopatry. The coexistence of lineages within sites may reflect density‐dependent attack by species‐specific strains of pathogenic fungi and/or root‐nodulating bacteria specializing on distinct genotypes.     

Along the speciation continuum in sticklebacks

Speciation can be viewed as a continuum, potentially divisible into several states: (1) continuous variation within panmictic populations, (2) partially discontinuous variation with minor reproductive isolation, (3) strongly discontinuous variation with strong but reversible reproductive isolation and (4) complete and irreversible reproductive isolation. Research on sticklebacks (Gasterosteidae) reveals factors that influence progress back and forth along this continuum, as well as transitions between the states. Most populations exist in state 1, even though some of these show evidence of disruptive selection and positive assortative mating. Transitions to state 2 seem to usually involve strong divergent selection coupled with at least a bit of geographic separation, such as parapatry (e.g. lake and stream pairs and mud and lava pairs) or allopatry (e.g. different lakes). Transitions to state 3 can occur when allopatric or parapatric populations that evolved under strong divergent selection come into secondary contact (most obviously the sympatric benthic and limnetic pairs), but might also occur between populations that remained in parapatry or allopatry. Transitions to state 4 might be decoupled from these selective processes, because the known situations of complete, or nearly complete, reproductive isolation (Japan Sea and Pacific Ocean pair and the recognized gasterosteid species) are always associated with chromosomal rearrangements and environment‐independent genetic incompatibilities. Research on sticklebacks has thus revealed complex and shifting interactions between selection, adaptation, mutation and geography during the course of speciation.     

SINGLE‐GENE SPECIATION WITH PLEIOTROPY: EFFECTS OF ALLELE DOMINANCE,POPULATION SIZE,AND DELAYED INHERITANCE

Single‐gene speciation is considered to be unlikely, but an excellent example is found in land snails, in which a gene for left‐right reversal has given rise to new species multiple times. This reversal might be facilitated by their small population sizes and maternal effect (i.e., “delayed inheritance,” in which an individual's phenotype is determined by the genotype of its mother). Recent evidence suggests that a pleiotropic effect of the speciation gene on antipredator survival may also promote speciation. Here we theoretically demonstrate that, without a pleiotropic effect, in small populations the fixation probability of a recessive mutant is higher than a dominant mutant, but they are identical for large populations and sufficiently weak selection. With a pleiotropic effect that increases mutant viability, a dominant mutant has a higher fixation probability if the strength of viability selection is sufficiently greater than that of reproductive incompatibility, whereas a recessive mutant has a higher fixation probability otherwise. Delayed inheritance increases the fixation probability of a mutant if viability selection is sufficiently weaker than reproductive incompatibility. Our results clarify the conflicting effects of viability selection and positive frequency‐dependent selection due to reproductive incompatibility and provide a new perspective to single‐gene speciation theory.     

GENETICS OF INCIPIENT SPECIATION IN DROSOPHILA MOJAVENSIS. III. LIFE‐HISTORY DIVERGENCE IN ALLOPATRY AND REPRODUCTIVE ISOLATION

We carried out a three‐tiered genetic analysis of egg‐to‐adult development time and viability in ancestral and derived populations of cactophilic Drosophila mojavensis to test the hypothesis that evolution of these life‐history characters has shaped premating reproductive isolation in this species. First, a common garden experiment with 11 populations from Baja California and mainland Mexico and Arizona reared on two host species revealed significant host plant X region and population interactions for viability and development time, evidence for host plant adaptation. Second, replicated line crosses with flies reared on both hosts revealed autosomal, X chromosome, cytoplasmic, and autosome X cactus influences on development time. Viability differences were influenced by host plants, autosomal dominance, and X chromosomal effects. Many of the F₁, F₂, and backcross generations showed evidence of heterosis for viability. Third, a QTL analysis of male courtship song and epicuticular hydrocarbon variation based on 1688 Baja × mainland F₂ males also revealed eight QTL influencing development time differences. Mainland alleles at six of these loci were associated with longer development times, consistent with population‐level differences. Eight G × E interactions were also detected caused by longer development times of mainland alleles expressed on a mainland host with smaller differences among Baja genotypes reared on the Baja host plant. Four QTL influenced both development time and epicuticular hydrocarbon differences associated with courtship success, and there was a significant QTL‐based correlation between development time and cuticular hydrocarbon variation. Thus, the regional shifts in life histories that evolved once D. mojavensis invaded mainland Mexico from Baja California by shifting host plants were genetically correlated with variation in cuticular hydrocarbon‐based mate preferences.     

The Darwinian stickleback Gasterosteus aculeatus: a history of evolutionary studies*

The history of studies on the taxonomy and evolutionary biology of the three‐spined stickleback Gasterosteus aculeatus from the 18th century to the present is reviewed. After the publication of Darwin's Origin of the Species, four important dates, 1925, 1947, 1967 and 2001, are identified as marking major gains in the understanding of the evolution of the diversity in morphological, life‐history, physiological and behavioural traits that characterizes G. aculeatus. The period 1925–1970 led to the identification of the main themes of research: status and adaptive significance of lateral‐plate morphs; inter and intrapopulation trait variation in freshwater resident G. aculeatus and the adaptive significance of the variation. Between 1970 and 2001, these themes were investigated using variation observed particularly along the Pacific coast of the U.S.A. and Canada, notably in the Cook Inlet region of Alaska and the Haida Gwaii Archipelago. Studies on adaptive radiation and reproductive isolation in lacustrine, ecomorph pairs (limnetics and benthics) discovered in the Strait of Georgia region have been particularly productive. From 2001, the application of genomic studies to these problems began to open up the study of the relationships between genotype, phenotype and selective advantage to causal analysis.     

Differential rates of morphological divergence in birds

There are more small-bodied bird species than there are large-bodied, even on a logarithmic scale. In birds this pattern, which is also found in other higher taxa, appears not to be due to neutral evolution. It has often been suggested that the skew of body size frequency distributions is the result of a relationship between body size and the net rate of speciation, but phylogenetic analyses so far have rejected the hypothesis that small-bodied species are subject to higher net rates of speciation. On the contrary, we show that there exists a relationship between body size and its own evolutionary variability: avian families of small body size show less interspecific variation in body size than large-bodied families of similar age and species richness.     

Consequences of divergence and introgression for speciation in Andean cloud forest birds

Divergence with gene flow is well documented and reveals the influence of ecological adaptation on speciation. Yet, it remains intuitive that gene exchange inhibits speciation in many scenarios, particularly among ecologically similar populations. The influence of gene flow on the divergence of populations facing similar selection pressures has received less empirical attention than scenarios where differentiation is coupled with local environmental adaptation. I used a paired study design to test the influence of genomic divergence and introgression on plumage differentiation between ecologically similar allopatric replacements of Andean cloud forest birds. Through analyses of short‐read genome‐wide sequences from over 160 individuals in 16 codistributed lineages, I found that plumage divergence is associated with deep genetic divergence, implicating a prominent role of geographic isolation in speciation. By contrast, lineages that lack plumage divergence across the same geographic barrier are more recently isolated or exhibit a signature of secondary genetic introgression, indicating a negative relationship between gene flow and divergence in phenotypic traits important to speciation. My results suggest that the evolutionary outcomes of cycles of isolation and divergence in this important theatre of biotic diversification are sensitive to time spent in the absence of gene flow.     

The geography of mammalian speciation: mixed signals from phylogenies and range maps

The importance of geographic isolation in speciation has been debated since the 19th century. Since the beginning of the 20th century, the consensus has been that most speciation involves divergence in allopatry. This consensus was based largely on decades of observations by naturalists and verbal arguments against speciation without isolation. Recent attempts to quantify the importance of allopatric versus sympatric speciation using comparative methods called "age-range correlation" (ARC) suggest that allopatric speciation is more common than sympatric speciation. However, very few taxa have been studied and there are concerns about the adequacy of the methods. We propose methodological improvements including changes in the way overlap between clades is quantified and Monte Carlo methods to test the null hypothesis of no relationship between phylogenetic relatedness and geographic range overlap. We analyze 14 clades of mammals, chosen because of the availability of data and the consensus among mammalogists that speciation is routinely allopatric. Although data from a few clades clearly indicate allopatric speciation, divergence with gene flow is plausible in others and many results are inconclusive. The relative rarity of significant correlations between phylogenetic distance and range overlap may have three distinct causes: (1) post-speciation range changes, (2) relative rarity of range overlap, and (3) a mixture of geographic modes of speciation. Our results support skepticism about ARC's power for inferring the biogeography of speciation. Yet, even if few clades provide clear signals, meta-analytic approaches such as ARC may set bounds on the prevalence of alternative modes of speciation.     

Novel trophic niches drive variable progress towards ecological speciation within an adaptive radiation of pupfishes

Adaptive radiation is recognized by a rapid burst of phenotypic, ecological and species diversification. However, it is unknown whether different species within an adaptive radiation evolve reproductive isolation at different rates. We compared patterns of genetic differentiation between nascent species within an adaptive radiation of Cyprinodon pupfishes using genotyping by sequencing. Similar to classic adaptive radiations, this clade exhibits rapid morphological diversification rates and two species are novel trophic specialists, a scale‐eater and hard‐shelled prey specialist (durophage), yet the radiation is <10 000 years old. Both specialists and an abundant generalist species all coexist in the benthic zone of lakes on San Salvador Island, Bahamas. Based on 13 912 single‐nucleotide polymorphisms (SNPs), we found consistent differences in genetic differentiation between each specialist species and the generalist across seven lakes. The scale‐eater showed the greatest genetic differentiation and clustered by species across lakes, whereas durophage populations often clustered with sympatric generalist populations, consistent with parallel speciation across lakes. However, we found strong evidence of admixture between durophage populations in different lakes, supporting a single origin of this species and genome‐wide introgression with sympatric generalist populations. We conclude that the scale‐eater is further along the speciation‐with‐gene‐flow continuum than the durophage and suggest that different adaptive landscapes underlying these two niche environments drive variable progress towards speciation within the same habitat. Our previous measurements of fitness surfaces in these lakes support this conclusion: the scale‐eating fitness peak may be more distant than the durophage peak on the complex adaptive landscape driving adaptive radiation.