Species-independent, geographical structuring of chloroplast DNA haplotypes in a montane herb Ipomopsis (Polemoniaceae)

Two hypotheses have been proposed to explain the occurrence of hybrid zones between red-flowered Ipomopsis aggregata and white-flowered I. tenuituba . Either local adaptation to hummingbird and hawkmoth pollinators has given rise to sympatric (or parapatric) divergence of flower colour and morphology (primary intergradation at hybrid zones), or alternatively two previously allopatric species are coming into contact at several geographical areas of secondary intergradation. We examined restriction site patterns in nuclear DNA (nrDNA), chloroplast DNA (cpDNA) and mitochondrial DNA (mtDNA) from populations of I. aggregata and I. tenuituba representing seven zones of sympatry. No variation was detected in a 350-bp fragment of mtDNA and uninformative levels of variation were observed for nrDNA. We detected 22 potentially informative restriction site polymorphisms in cpDNA, all of which united geographical areas containing populations of both species. We detected no informative species-specific markers. Studies of other species (e.g. oaks) have detected similar species-independent geographical structure of cpDNA. However, in these cases secondary interegradation could be inferred from species-specific nuclear alleles. The pattern in Ipomopsis is consistent with both primary intergradation (independent speciation in each area of sympatry) or secondary intergradation involving complete cytoplasmic replacement. Thus, additional data are needed to explain the origin of hybrid zones in Ipomopsis .     

Genetic structure and bio-climatic modeling support allopatric over parapatric speciation along a latitudinal gradient

ABSTRACT: BACKGROUND: Four of the five species of Telopea (Proteaceae) are distributed in a latitudinal replacement pattern on the south-eastern Australian mainland. In similar circumstances, a simple allopatric speciation model that identifies the origins of genetic isolation within temporal geographic separation is considered as the default model. However, secondary contact between differentiated lineages can result in similar distributional patterns to those arising from a process of parapatric speciation (where gene flow between lineages remains uninterrupted during differentiation). Our aim was to use the characteristic distributional patterns in Telopea to test whether it reflected the evolutionary models of allopatric or parapatric speciation. Using a combination of genetic evidence and environmental niche modelling, we focused on three main questions: do currently described geographic borders coincide with genetic and environmental boundaries; are there hybrid zones in areas of secondary contact between closely related species; did species distributions contract during the last glacial maximum resulting in distributional gaps even where overlap and hybridisation currently occur? RESULTS: Total genomic DNA was extracted from 619 individuals sampled from 36 populations representing the four species. Seven nuclear microsatellites (nSSR) and six chloroplast microsatellites (cpSSR) were amplified across all populations. Genetic structure and the signature of admixture in overlap zones was described using the Bayesian clustering methods implemented in STUCTURE and NewHybrids respectively. Relationships between chlorotypes were reconstructed as a median-joining network. Environmental niche models were produced for all species using environmental parameters from both the present day and the last glacial maximum (LGM). The nSSR loci amplified a total of 154 alleles, while data for the cpSSR loci produced a network of six chlorotypes. STRUCTURE revealed an optimum number of five clusters corresponding to the four recognised species with the additional division of T. speciosissima into populations north and south of the Shoalhaven River valley. Unexpectedly, the northern disjunct population of T. oreades grouped with T. mongaensis and was identified as a hybrid swarm by the Bayesian assignment test implemented in NewHybrids. Present day and LGM environmental niche models differed dramatically, suggesting that distributions of all species had repeatedly expanded and contracted in response to Pleistocene climatic oscillations and confirming strongly marked historical distributional gaps among taxes. CONCLUSIONS: Genetic structure and bio-climatic modeling results are more consistent with a history of allopatric speciation followed by repeated episodes of secondary contact and localised hybridisation, rather than with parapatric speciation. This study on Telopea shows that the evidence for temporal exclusion of gene flow can be found even outside obvious geographical contexts, and that it is possible to make significant progress towards excluding parapatric speciation as a contributing evolutionary process.     

Evaluating mechanisms of diversification in a Guineo‐Congolian tropical forest frog using demographic model selection

The accumulation of biodiversity in tropical forests can occur through multiple allopatric and parapatric models of diversification, including forest refugia, riverine barriers and ecological gradients. Considerable debate surrounds the major diversification process, particularly in the West African Lower Guinea forests, which contain a complex geographic arrangement of topographic features and historical refugia. We used genomic data to investigate alternative mechanisms of diversification in the Gaboon forest frog, Scotobleps gabonicus, by first identifying population structure and then performing demographic model selection and spatially explicit analyses. We found that a majority of population divergences are best explained by allopatric models consistent with the forest refugia hypothesis and involve divergence in isolation with subsequent expansion and gene flow. These population divergences occurred simultaneously and conform to predictions based on climatically stable regions inferred through ecological niche modelling. Although forest refugia played a prominent role in the intraspecific diversification of S. gabonicus, we also find evidence for potential interactions between landscape features and historical refugia, including major rivers and elevational barriers such as the Cameroonian Volcanic Line. We outline the advantages of using genomewide variation in a model‐testing framework to distinguish between alternative allopatric hypotheses, and the pitfalls of limited geographic and molecular sampling. Although phylogeographic patterns are often species‐specific and related to life‐history traits, additional comparative studies incorporating genomic data are necessary for separating shared historical processes from idiosyncratic responses to environmental, climatic and geological influences on diversification.     

Some genetic consequences of ice ages, and their role, in divergence and speciation

The genetic effects of pleistocene ice ages are approached by deduction from paleoenvironmental information, by induction from the genetic structure of populations and species, and by their combination to infer likely consequences. (1) Recent palaeoclimatic information indicate rapid global reversals and changes in ranges of species which would involve elimination with spreading from the edge. Leading edge colonization during a rapid expansion would be leptokurtic and lead to homozygosity and spatial assortment of genomes. In Europe and North America, ice age contractions were into southern refugia, which would promote genome reorganization. (2) The present day genetic structure of species shows frequent geographic subdivision, with parapatric genomes, hybrid zones and suture zones. A survey of recent DNA phylogeographic information supports and extends earlier work. (3) The grasshopper Chorthippus parallelus is used to illustrate such data and processes. Its range in Europe is divided on DNA sequences into five parapatric races, with southern genomes showing greater haplotype diversity - probably due to southern mountain blocks acting as refugia and northern expansion reducing diversity. (4) Comparison with other recent studies shows a concordance of such phylogeographic data over pleistocene time scales. (5) The role that ice age range changes may have played in changing adaptations is explored, including the limits of range, rapid change in new invasions and refugial differentiation in a variety of organisms. (6) The effects of these events in causing divergence and speciation are explored using Chorthippus as a paradigm. Repeated contraction and expansion would accumulate genome differences and adaptations, protected from mixing by hybrid zones, and such a composite mode of speciation could apply to many organisms.     

Genetic surfing,not allopatric divergence,explains spatial sorting of mitochondrial haplotypes in venomous coralsnakes

Strong spatial sorting of genetic variation in contiguous populations is often explained by local adaptation or secondary contact following allopatric divergence. A third explanation, spatial sorting by stochastic effects of range expansion, has been considered less often though theoretical models suggest it should be widespread, if ephemeral. In a study designed to delimit species within a clade of venomous coralsnakes, we identified an unusual pattern within the Texas coral snake (Micrurus tener): strong spatial sorting of divergent mitochondrial (mtDNA) lineages over a portion of its range, but weak sorting of these lineages elsewhere. We tested three alternative hypotheses to explain this pattern—local adaptation, secondary contact following allopatric divergence, and range expansion. Collectively, near panmixia of nuclear DNA, the signal of range expansion associated sampling drift, expansion origins in the Gulf Coast of Mexico, and species distribution modeling suggest that the spatial sorting of divergent mtDNA lineages within M. tener has resulted from genetic surfing of standing mtDNA variation—not local adaptation or allopatric divergence. Our findings highlight the potential for the stochastic effects of recent range expansion to mislead estimations of population divergence made from mtDNA, which may be exacerbated in systems with low vagility, ancestral mtDNA polymorphism, and male‐biased dispersal.     

Lack of congruence of genetic and niche divergence in Podarcis hispanicus complex

Niche divergence among closely related lineages can be informative on the ecological and evolutionary processes involved in differentiation, particularly in the case of cryptic species complexes. Here we compared phylogenetic relationships and niche similarity between pairs of lineages included in the Podarcis hispanicus complex to examine patterns of niche divergence and its role in the organization of current diversity patterns, as allopatric, parapatric, and sympatric lineages occur in the Western Mediterranean Basin. First, we used ecological niche models to characterize the realized climatic niche of each Podarcis hispanicus complex lineage based on topographic and climatic variables, to identify important variables, and to test for niche conservatism or divergence between pairs of lineages. Variables related to precipitation generally exhibited the highest contribution to niche models, highlighting the importance of rainfall levels in shaping distributions of Podarcis wall lizards. We found that most forms have significant differences in realized climatic niches that do not follow the pattern of mitochondrial divergence. These results lend support to the hypothesis that genetic divergence across Podarcis hispanicus complex most likely occurred in allopatric conditions, mostly with significant niche divergence. Competition after secondary contact is also suggested by the common occurrence of niche overlap between lineages that exhibit strictly parapatric distribution. The almost continuous distribution of Podarcis lizards in the study area appears to be a result of a combination of complementary suitable niches and competition, which seem two important mechanisms limiting geographic distributions and restricting the existence of extensive contact zones.     

Allopatric divergence, secondary contact, and genetic isolation in wild yeast populations

In plants and animals, new biological species clearly have arisen as a byproduct of genetic divergence in allopatry. However, our understanding of the processes that generate new microbial species remains limited [1] despite the large contribution of microbes to the world's biodiversity. A recent hypothesis claims that microbes lack biogeographical divergence because their population sizes are large and their migration rates are presumably high [2, 3]. In recapitulating the classic microbial-ecology dictum that "everything is everywhere, and the environment selects"[4, 5], this hypothesis casts doubt on whether geographic divergence promotes speciation in microbes. To date, its predictions have been tested primarily with data from eubacteria and archaebacteria [6-8]. However, this hypothesis's most important implication is in sexual eukaryotic microbes, where migration and genetic admixture are specifically predicted to inhibit allopatric divergence and speciation [9]. Here, we use nuclear-sequence data from globally distributed natural populations of the yeast Saccharomyces paradoxus to investigate the role of geography in generating diversity in sexual eukaryotic microbes. We show that these populations have undergone allopatric divergence and then secondary contact without genetic admixture. Our data thus support the occurrence of evolutionary processes necessary for allopatric speciation in sexual microbes.     

Phylogeography of a widespread lizard complex reflects patterns of both geographic and ecological isolation

A primary challenge for modern phylogeography is understanding how ecology and geography, both contemporary and historical, shape the spatial distribution and evolutionary histories of species. Phylogeographic patterns are the result of many factors, including geology, climate, habitat, colonization history and lineage‐specific constraints. Assessing the relative influences of these factors is difficult because few species, regions and environments are sampled in enough detail to compare competing hypotheses rigorously and because a particular phylogeographic pattern can potentially result from different evolutionary scenarios. The silky anoles (Anolis sericeus complex) of Central America and Mexico are abundant and found in all types of lowland terrestrial habitat, offering an excellent opportunity to test the relative influences of the factors affecting diversification. Here, we performed a range‐wide statistical phylogeographic analysis on restriction site‐associated DNA (RAD) markers from silky anoles and compared the phylogeographic patterns we recovered to historical and contemporary environmental and topographic data. We constructed niche models to compare niche overlap between sister lineages and conducted coalescent simulations to characterize how the major lineages of silky anoles have diverged. Our results revealed that the mode of divergence for major lineage diversification events was geographic isolation, resulting in ecological divergence between lineages, followed by secondary contact. Moreover, comparisons of parapatric sister lineages suggest that ecological niche divergence contributed to isolation by environment in this system, reflecting the natural history differences among populations in divergent environments.     

Spatial and host related genomic variation in partially sympatric cactophagous moth species

Surveys of patterns of genetic variation in natural sympatric and allopatric populations of recently diverged species are necessary to understand the processes driving intra- and interspecific diversification. The South American moths Cactoblastis cactorum, Cactoblastis doddi and Cactoblastis bucyrus are specialized in the use of cacti as host plants. These species have partially different geographic ranges and differ in patterns of host plant use. However, there are areas that overlap, particularly, in northwestern Argentina, where they are sympatric. Using a combination of genome-wide SNPs and mitochondrial data we assessed intra and interspecific genetic variation and investigated the relative roles of geography and host plants on genetic divergence. We also searched for genetic footprints of hybridization between species. We identified three well delimited species and detected signs of hybridization in the area of sympatry. Our results supported a hypothetical scenario of allopatric speciation in the generalist C. cactorum and genetic interchange during secondary geographic contact with the pair of specialists C. bucyrus and C. doddi that probably speciated sympatrically. In both cases, adaptation to new host plants probably played an important role in speciation. The results also suggested the interplay of geography and host plant use as drivers of divergence and limiting gene flow at intra and interspecific levels.     

Genetic divergence and introgressive hybridization betweenAlnus sinuata andA. crispa (Betulaceae)

The actinorhizal genusAlnus contains numerous taxa that have been morphologically classified into different subgenera, species and subspecies. The genetic divergence has been evaluated within subg.Alnobetula between the parapatric taxaAlnus sinuata andA. crispa, using diversity of allozyme markers at 15 structural loci among 20 populations. Evidence for introgressive hybridization at the overlap of their ranges was noted in three populations. However, the width of the hybrid zone appeared tenuous. The average genetic distance derived from the comparisons of conspecific populations was much smaller than the interspecific distance (D = 0.047). This allelic divergence was also paralleled with larger amounts of allelic and genotypic diversity within and among populations ofA. sinuata, which are occupying a more heterogenous ecological niche. It is proposed that the repeated advances and retreats of the ice sheet during the Pleistocene may have promoted the divergence and allopatric evolution of these subspecies, and that secondary contact may have occurred repeatedly during the interglacial periods. The dynamic-equilibrium model would predict in such cases that narrow hybrid zones, formed at the contact of parapatric ranges, would impede gene exchange between parental taxa by selection against hybrids. The results obtained in this study seemed concordant with this hypothesis, as they were also in agreement with the existent taxonomical treatment of these taxa based on morphology.     

Hybridization between two gartersnake species (<Emphasis Type="Italic">Thamnophis</Emphasis>) of conservation concern: a threat or an important natural interaction?

Distinguishing between hybrid zones formed by secondary contact versus parapatric divergence-with-gene-flow is an important challenge for understanding the interplay of geographic isolation and local adaptation in the origin of species. Similarly, distinguishing between natural hybrid zones and those that formed as a consequence of recent human activities has important conservation implications. Recent work has demonstrated the existence of a narrow hybrid zone between the plains gartersnake (Thamnophis radix) and Butler’s gartersnake (T. butleri) in the Great Lakes region of North America, raising questions about the history and conservation value of genetically admixed populations. Both taxa are of conservation concern, and it is not clear whether to regard hybridization as a threat or a natural interaction. Here we use phylogeographic and population genetic methods to assess the timescales of divergence and hybridization, and test for evidence that the hybrid zone is of recent origin. We assayed AFLP markers and ND2 mitochondrial DNA (mtDNA) sequences from T. radix, T. butleri, and the closely related short-headed gartersnake (T. brachystoma) throughout their North American ranges. We find shallow mtDNA divergence overall and high levels of variation within the contact zone. These patterns are inconsistent with recent contact of long-diverged taxa. It is not possible to distinguish true divergence-with-gene-flow from a long-term secondary contact zone, but we infer that the hybrid zone is a long-standing, natural interaction.     

Mitochondrial and Nuclear Genes-Based Phylogeography of Arvicanthis niloticus (Murinae) and Sub-Saharan Open Habitats Pleistocene History

A phylogeographic study was conducted on the Nile grass rat, Arvicanthis niloticus, a rodent species that is tightly associated with open grasslands from the Sudano-Sahelian regions. Using one mitochondrial (cytochrome b) and one nuclear (intron 7 of Beta Fibrinogen) gene, robust patterns were retrieved that clearly show that (i) the species originated in East Africa concomitantly with expanding grasslands some 2 Ma, and (ii) four parapatric and genetically well-defined lineages differentiated essentially from East to West following Pleistocene bioclimatic cycles. This strongly points towards allopatric genetic divergence within savannah refuges during humid episodes, then dispersal during arid ones; secondary contact zones would have then stabilized around geographic barriers, namely, Niger River and Lake Chad basins. Our results pertinently add to those obtained for several other African rodent as well as non-rodent species that inhabit forests, humid zones, savannahs and deserts, all studies that now allow one to depict a more comprehensive picture of the Pleistocene history of the continent south of the Sahara. In particular, although their precise location remains to be determined, at least three Pleistocene refuges are identified within the West and Central African savannah biome.     

Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses

Statistical phylogeographic studies contribute to our understanding of the factors that influence population divergence and speciation, and that ultimately generate biogeographical patterns. The use of coalescent modelling for analyses of genetic data provides a framework for statistically testing alternative hypotheses about the timing and pattern of divergence. However, the extent to which such approaches contribute to our understanding of biogeography depends on how well the alternative hypotheses chosen capture relevant aspects of species histories. New modelling techniques, which explicitly incorporate spatio-geographic data external to the gene trees themselves, provide a means for generating realistic phylogeographic hypotheses, even for taxa without a detailed fossil record. Here we illustrate how two such techniques – species distribution modelling and its historical extension, palaeodistribution modelling – in conjunction with coalescent simulations can be used to generate and test alternative hypotheses. In doing so, we highlight a few key studies that have creatively integrated both historical geographic and genetic data and argue for the wider incorporation of such explicit integrations in biogeographical studies.     

Increased genetic divergence between two closely related fir species in areas of range overlap

Because of introgressive hybridization, closely related species can be more similar to each other in areas of range overlap (parapatry or sympatry) than in areas where they are geographically isolated from each other (allopatry). Here, we report the reverse situation based on nuclear genetic divergence between two fir species, Abies chensiensis and Abies fargesii, in China, at sites where they are parapatric relative to where they are allopatric. We examined genetic divergence across 126 amplified fragment length polymorphism (AFLP) markers in a set of 172 individuals sampled from both allopatric and parapatric populations of the two species. Our analyses demonstrated that AFLP divergence was much greater between the species when comparisons were made between parapatric populations than between allopatric populations. We suggest that selection in parapatry may have largely contributed to this increased divergence.     

Patterns and processes in the genetic differentiation of the Brachionus calyciflorus complex, a passively dispersing freshwater zooplankton

Elucidating the evolutionary patterns and processes of extant species is an important objective of any research program that seeks to understand population divergence and, ultimately, speciation. The island-like nature and temporal fluctuation of limnetic habitats create opportunities for genetic differentiation in rotifers through space and time. To gain further understanding of spatio-temporal patterns of genetic differentiation in rotifers other than the well-studied Brachionus plicatilis complex in brackish water, a total of 318 nrDNA ITS sequences from the B. calyciflorus complex in freshwater were analysed using phylogenetic and phylogeographic methods. DNA taxonomy conducted by both the sequence divergence and the GMYC model suggested the occurrence of six potential cryptic species, supported also by reproductive isolation among the tested lineages. The significant genetic differentiation and non-significant correlation between geographic and genetic distances existed in the most abundant cryptic species, BcI-W and Bc-SW. The large proportion of genetic variability for cryptic species Bc-SW was due to differences between sampling localities within seasons, rather than between different seasons. Nested Clade Analysis suggested allopatric or past fragmentation, contiguous range expansion and long-distance colonization possibly coupled with subsequent fragmentation as the probable main forces shaping the present-day phylogeographic structure of the B. calyciflorus species complex.     

Hybridization during altitudinal range shifts: nuclear introgression leads to extensive cyto‐nuclear discordance in the fire salamander

Ecological models predict that, in the face of climate change, taxa occupying steep altitudinal gradients will shift their distributions, leading to the contraction or extinction of the high‐elevation (cold‐adapted) taxa. However, hybridization between ecomorphologically divergent taxa commonly occurs in nature and may lead to alternative evolutionary outcomes, such as genetic merger or gene flow at specific genes. We evaluate this hypothesis by studying patterns of divergence and gene flow across three replicate contact zones between high‐ and low‐elevation ecomorphs of the fire salamander (Salamandra salamandra) that have experienced altitudinal range shifts over the current postglacial period. Strong population structure with high genetic divergence in mitochondrial DNA suggests that vicariant evolution has occurred over several glacial–interglacial cycles and that it has led to cryptic differentiation within ecomorphs. In current parapatric boundaries, we do not find evidence for local extinction and replacement upon postglacial expansion. Instead, parapatric taxa recurrently show discordance between mitochondrial and nuclear markers, suggesting nuclear‐mediated gene flow across contact zones. Isolation with migration models support this hypothesis by showing significant gene flow across all five parapatric boundaries. Together, our results suggest that, while some genomic regions, such as the mitochondria, may follow morphologic species traits and retreat to isolated mountain tops, other genomic regions, such as nuclear markers, may flow across parapatric boundaries, sometimes leading to a complete genetic merger. We show that despite high ecologic and morphologic divergence over prolonged periods of time, hybridization allows for evolutionary outcomes alternative to extinction and replacement of taxa in response to climate change.     

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.     

Host-related genetic differentiation in the anther smut fungus Microbotryum violaceum in sympatric, parapatric and allopatric populations of two host species Silene latifolia and S. dioica

We investigated genetic diversity in West European populations of the fungal pathogen Microbotryum violaceum in sympatric, parapatric and allopatric populations of the host species Silene latifolia and S. dioica, using four polymorphic microsatellite loci. In allopatric host populations, the fungus was highly differentiated by host species, exhibiting high values of F(ST) and R(ST), and revealed clear and distinct host races. In sympatric and parapatric populations we found significant population differentiation as well, except for one sympatric population in which the two host species grew truly intermingled. The mean number of alleles per locus for isolates from each of the host species was significantly higher in sympatric/parapatric than in allopatric populations. This suggests that either gene flow between host races in sympatry, or in case of less neutral loci, selection in a more heterogeneous host environment can increase the level of genetic variation in each of the demes. The observed pattern of host-related genetic differentiation among these geographically spread populations suggest a long-term divergence between these host races. In sympatric host populations, both host races presumably come in secondary contact, and host-specific alleles are exchanged depending on the amount of fungal gene flow.     

Testing the role of climate in speciation: New methods and applications to squamate reptiles (lizards and snakes)

Climate may play important roles in speciation, such as causing the range fragmentation that underlies allopatric speciation (through niche conservatism) or driving divergence of parapatric populations along climatic gradients (through niche divergence). Here, we developed new methods to test the frequency of climate niche conservatism and divergence in speciation, and applied it to species pairs of squamate reptiles (lizards and snakes). We used a large‐scale phylogeny to identify 242 sister species pairs for analysis. From these, we selected all terrestrial allopatric pairs with sufficient occurrence records (n = 49 pairs) and inferred whether each originated via climatic niche conservatism or climatic niche divergence. Among the 242 pairs, allopatric pairs were most common (41.3%), rather than parapatric (19.4%), partially sympatric (17.7%), or fully sympatric species pairs (21.5%). Among the 49 selected allopatric pairs, most appeared to have originated via climatic niche divergence (61–76%, depending on the details of the methods). Surprisingly, we found greater climatic niche divergence between allopatric sister species than between parapatric pairs, even after correcting for geographic distance. We also found that niche divergence did not increase with time, further implicating niche divergence in driving lineage splitting. Overall, our results suggest that climatic niche divergence may often play an important role in allopatric speciation, and the methodology developed here can be used to address the generality of these findings in other organisms.     

The geography of divergence with gene flow facilitates multitrait adaptation and the evolution of pollinator isolation in Mimulus aurantiacus

Ecological adaptation is the driving force during divergence with gene flow and generates reproductive isolation early in speciation. Although gene flow opposes divergence, local adaptation can be facilitated by factors that prevent the breakup of favorable allelic combinations. We investigated how selection, genetic architecture, and geography have contributed to the maintenance of floral trait divergence and pollinator isolation between parapatric ecotypes of Mimulus aurantiacus. Combining greenhouse, field, and genomic studies, we show that sharp clines in floral traits are maintained by spatially varying selection. Although adaptation breaks down where the ecotypes co‐occur, leading to the formation of a hybrid zone, the largely non‐overlapping distributions of the ecotypes shield them from immigrant genes, facilitating divergence across most of the range. In contrast to the sharp genetic discontinuities observed across most hybrid zones, we observed a gradual cline in genome‐wide divergence and a pattern of isolation by distance across the landscape. Thus, contrary to a long period of allopatry followed by recent re‐contact, our data suggest that floral trait divergence in M. aurantiacus may have evolved with locally restricted, but ongoing gene flow. Therefore, our study reveals how the geographic distribution of an organism can contribute to the evolution of premating isolation in the early stages of divergence with gene flow.