What is the meaning of 'primary' and 'secondary' sympatric speciation in this paper?

What is the meaning of 'primary' and 'secondary' sympatric speciation in this paper?

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Sympatric Speciation in the Genomic Era. Both terms are used throughout the paper.

I'm not able to make sense of these terms in the contexts used.

I've also heard the terms 'primary' and 'secondary' gene flow elsewhere on the same topic - are they related?

From the abstract:

However, I argue that genomic studies based on contemporary populations may never be able to provide unequivocal evidence of true primary sympatric speciation, and there is a need to incorporate palaeogenomic studies in to this field. This inability to robustly distinguish cases of primary and secondary divergence-with-gene-flow may be inconsequential, as both are useful for understanding the role of large effect barrier loci in the progression from localised genic isolation to genome-wide reproductive isolation. I argue that they can be of equivalent interest due to shared underlying mechanisms driving divergence and potentially leaving similar coalescent patterns.

From the introduction:

Lastly, I consider whether primary and secondary sympatric speciation represent a mechanistic dichotomy, I suggest that primary and secondary contact can leave a similar genomic signature, when speciation is driven by tightly clustered or large effect loci. Arguably, the advent of affordable population genomic studies should place less focus on whether study systems result from primary or secondary contact and instead focus on the mechanistic aspects of the genomic architecture and making progress in identifying the conditions and processes under which natural and sexual selection can drive speciation, without extrinsic barriers to gene flow.


Sympatric speciation and allopatric speciation with later migration into the same habitat were historically diffucult to distinguish without looking at palaeo-biological data. The paper argues that while palaeo-genetics has made this easier, it is still difficult to distinguish pure sympatric speciation (which it calls primary) and sympatric speciation with a geneflow from an geographically separated (allopatrically speciated?) subpopulation (which it terms "secondary sympatric speciation" or "speciation with secondary gene flow", "… with secondary contact" etc.).


Speciation is the divergence of one species (with one gene pool) into two different species (with different gene pools). It is obvious that this will happen if subpolulations are geographically separated and continue to adapt to their local conditions (allopatric speciation).

However, Mayr suggested (back in the 1940s) that there is another type of speciation that happens while the speciating populations share a habitat, and, consequently, while gene flow between these subpopulations is maintained until the speciation process is complete. This requires strong selection pressure towards two different ecological niches each with their associated adaptations.

Empirical examples have been discussed and called into question again. One cool and frequently discussed example is that of the apple maggot in North America that has developed from the hawthorn maggot after the introduction of apples in North America.


Unequivocal examples for pure sympatric speciation are rare, leading to some debate about the merits of the concept. Sympatric speciation models (following Maynard Smith's models from the 1960s) as well as the reasons for skepticism towards them are illustratively explained for instance in this article (Felsenstein 1980), page 133-135.

The debate continues, today with additional, newer findings from genetics, palaeo-genetics, etc. This is what the article in the OP (Foote, 2018) was about. The pdf of the article (Foote, 2018) without paywall can also be found here. While Foote suggests that what pure sympartic speciation and speciation with secondary gene flow may never be unequivocally distinguished (without additional palaeo-genetic information), others are more optimistic, e.g. Richards et al. 2019 (without paywall on biorxiv). Coincidentally, Richards et al. have a very nice illustration (their Figure 1) that illustrates the issue the OP was asking about.

Speciation: Definition and Types

7. Isolation: A genetic isolate is population of organisms that has little genetic mixing with other organisms within the same species. This may result in speciation, but this is not necessarily the case.

How do we get speciation?

Sympatric speciation occurs when populations of a species that share the same habitat become reproductively isolated from each other. This speciation phenomenon most commonly occurs through polyploidy, in which an offspring or group of offspring will be produced with twice the normal number of chromosomes.

What are the different types of speciation?

This is called allopatric speciation. There are four types of speciation: allopatric, peripatric, parapatric, and sympatric.

What are the four modes of speciation?

There are four geographic modes of speciation in nature, based on the extent to which speciating populations are isolated from one another: allopatric, peripatric, parapatric, and sympatric.

What is the Peripatric speciation?

Peripatric speciation is a mode of speciation in which a new species is formed from an isolated peripheral population. Since peripatric speciation resembles allopatric speciation, in that populations are isolated and prevented from exchanging genes, it can often be difficult to distinguish between them.

What is the difference between allopatric and sympatric speciation?

Thanks for reading Speciation: Definition and Types

Sympatric Speciation in the Post “Modern Synthesis” Era of Evolutionary Biology

Sympatric speciation is among the most controversial and challenging concepts in evolution. There are a multitude of definitions of speciation alone, and when combined with the biogeographic concept of sympatric range overlap, consensus on what sympatric speciation is, whether it happens, and its importance, is even more difficult to achieve. Providing the basis upon which to define and judge sympatric speciation, the Modern Evolutionary Synthesis (Huxley in Evolution: the modern synthesis. MIT Press, Cambridge, 1942) led to the conclusion that sympatric speciation is an inconsequential process in the generation of species diversity. In the post Modern Synthesis era of evolutionary biology, the PCR revolution and associated accumulation of DNA sequence data from natural populations has led to a resurgence of interest in sympatric speciation, and more importantly, the role of natural selection in lineage diversification. Much effort is currently being devoted to elucidating the processes by which the constituents of an initially panmictic population can become reproductively isolated and evolve some level of reproductive incompatibility without the complete cessation of gene flow due to geographic barriers. The evolution of reproductive isolation solely due to natural selection is perhaps the most controversial manner by which sympatric speciation occurs, and it is that which we focus upon in this review. Mathematical model simulations indicate that even strict definitions of sympatric speciation are possible to satisfy, empirical data consistent with sympatric divergence are accumulating, but irrefutable evidence of sympatric speciation in natural populations remains elusive. Genomic investigations are advancing our ability to identify genetic patterns caused by natural selection, thereby advancing our understanding of the power of natural selection relative to gene flow. Overall, sympatric lineage divergence, especially at the sub-species level, may have led to a substantial portion of biodiversity.

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Varying Rates of Speciation

Scientists around the world study speciation, documenting observations both of living organisms and those found in the fossil record. As their ideas take shape and as research reveals new details about how life evolves, they develop models to help explain rates of speciation. In terms of how quickly speciation occurs, two patterns are currently observed: gradual speciation model and punctuated equilibrium model.

In the gradual speciation model, species diverge gradually over time in small steps. In the punctuated equilibrium model, a new species undergoes changes quickly from the parent species, and then remains largely unchanged for long periods of time afterward (see the figure below). This early change model is called punctuated equilibrium, because it begins with a punctuated or periodic change and then remains in balance afterward. While punctuated equilibrium suggests a faster tempo, it does not necessarily exclude gradualism.

Art Connection

In (a) gradual speciation, species diverge at a slow, steady pace as traits change incrementally. In (b) punctuated equilibrium, species diverge quickly and then remain unchanged for long periods of time.

Which of the following statements is false?

  1. Punctuated equilibrium is most likely to occur in a small population that experiences a rapid change in its environment.
  2. Punctuated equilibrium is most likely to occur in a large population that lives in a stable climate.
  3. Gradual speciation is most likely to occur in species that live in a stable climate.
  4. Gradual speciation and punctuated equilibrium both result in the divergence of species.


Punctuated equilibrium is most likely to occur in a large population that lives in a stable climate.

The primary influencing factor on changes in speciation rate is environmental conditions. Under some conditions, selection occurs quickly or radically. Consider a species of snails that had been living with the same basic form for many thousands of years. Layers of their fossils would appear similar for a long time. When a change in the environment takes place—such as a drop in the water level—a small number of organisms are separated from the rest in a brief period of time, essentially forming one large and one tiny population. The tiny population faces new environmental conditions. Because its gene pool quickly became so small, any variation that surfaces and that aids in surviving the new conditions becomes the predominant form.

Results and Discussion

Nuclear and mtDNA Gene Trees. Of the 19 total nuclear loci analyzed in the study, 4 were determined to be duplicated loci and excluded from further analysis (P341, P2480, P70, and P2919, mapping to chromosomes 1, 3, 3, and 6, respectively). MP gene trees for the remaining 15 nuclear loci and mtDNA are shown in Fig. 2 and supporting information, which is published on the PNAS web site). None of the sequenced genes deviated significantly from a molecular clock ( Table 1 ). Nine of the 15 nuclear loci displayed evidence for possible recombination by the method of Hudson and Kaplan ( Table 1 ). However, exchange was limited to alleles within identified haplotype classes (i.e., M, S/N, or N) or within geographic populations (Altiplano or United States). The only exceptions were the loci P667, P1700, and P2473, where recombination occurred between major haplotypes within the U.S. population (see supporting information). As would be expected for a nonrecombinant molecule, there was no evidence for exchange among mtDNA sequences.

Gene Tree Topologies and RND. Gene tree topologies differed significantly between loci mapping to chromosomes 1-3 and those residing elsewhere in the genome ( Fig. 2 ). A summary of the differences is shown in Fig. 3 , where RNDs are plotted between major haplotype classes segregating at loci in Altiplano vs. U.S. flies. RNDs clustered into three groups, corresponding to deep, intermediate, and shallow divergence between Mexican and U.S. haplotypes. Loci tended to fall into different RND categories based on their chromosomal location. Loci mapping to chromosomes 1-3 had significantly greater RNDs than genes on other chromosomes. Six of the nine loci on chromosomes 1-3, as well as mtDNA, had RNDs Ϡ.63 between at least one pair of haplotypes segregating in the United States and Altiplano ( Table 1 ). Two of the three loci not displaying deep RNDs (P3072 and P667) showed low levels of disequilibrium, with linked allozymes differentiating the apple and hawthorn host races (standardized disequilibrium between P3072 and Aat-2, 0.077 P = 0.504 n = 75 scored chromosomes r value P667/Me, 0.117 P = 0.259 n = 92), suggesting possible weaker associations of these genes with inversions or targets of selection on chromosomes 1 and 2, respectively. In contrast, none of the six loci residing on chromosomes other than 1-3 possessed a deep RND ( Table 1 ). Indeed, the deepest RND for any of these six loci was 0.361 (P1700), which was shallower than P22, the third locus on chromosome 3 not possessing a deep RND. Four of the six loci not on chromosomes 1-3 also displayed shallow RNDs of π.16, not appreciably greater than values found segregating within haplotype classes for these loci within Altiplano and U.S. populations ( Fig. 2 ). No locus residing on chromosomes 1-3 possessed a shallow RND ( Table 1 ).

Distribution of RNDs for nuclear loci not residing on chromosomes 1-3 (black bars), for genes located on chromosomes 1-3 (white bars), and for mtDNA (gray bar). The list on the left gives the number of loci displaying shallow RNDs (π.16) for the six sequenced genes not mapping to chromosomes 1-3 vs. the nine genes that do. The list on the right gives the number of loci displaying deep RNDs (Ϡ.63). RND values for each locus are given in Table 1 . P values were determined by two-tailed Fisher's exact tests.

Implications of the Gene Trees: Isolation, Contact, and Differential Gene Flow. The tripartite distribution of RNDs for nuclear and mtDNA gene trees is consistent with a hypothesis that Mexican and U.S. fly populations have undergone two cycles of geographic isolation and differential introgression ( Fig. 4 ). The deep and congruent RNDs for six of the loci on chromosomes 1-3 and mtDNA suggest an initial population subdivision of a Mexican/U.S. common ancestor 𢒁.57 Mya based on an insect mtDNA clock (1.15 × 10 -8 substitutions per bp per year) (39). We propose that this initial isolation event was followed by a period of contact from 0.5-1 Mya, during which time gene flow was considerable. Extensive population mixing accounts for the large number of loci displaying intermediate RNDs, as well as for the establishment of adaptive clines for inversions on chromosome 1-3. We do not know the location or extent of the contact zone or clines when they first formed. However, we presume that ecological factors related to host phenology affected the clines in the past in a similar manner as they do currently. Loci residing in other regions of the genome not under selection moved readily between Mexican and Northern populations and recombined, accounting for the lack of deep RNDs for chromosome 4 and 5 loci. In contrast, mtDNA did not introgress during this or any subsequent period of contact.

Biogeographic model depicting two cycles of isolation and differential introgression between Mexican Altiplano and Northern (United States) populations of R. pomonella.

We hypothesize that the initial period of contact was followed by a second cycle of isolation and introgression ( Fig. 4 ). Gene flow was differential during the most recent contact period. Loci residing on chromosomes 4 and 5 tended to move readily between populations, accounting for the shallow RNDs observed for most (4/6 67%) of these genes ( Fig. 3 and Table 1 ). In comparison, loci on chromosomes 1-3 did not introgress, resulting in a lack of shallow RNDs. The pattern of gene flow suggests that genetic differences accumulated on chromosomes 1-3 during the second isolation period. To the extent that these changes are defined by inversions (a supposition supported by genetic cross data and population-level linkage disequilibrium values within U.S. populations), they concur with rearrangement models of chromosomal speciation (9, 31). Also, the accumulation of additional inversion changes after the hypothesized time when clines were first established suggests that not all diapause-related differences among U.S. flies trace to Mexican origins.

Alternative Hypotheses for the Gene Trees. The pattern of differentiation seen for nuclear loci could potentially also be explained by incomplete linage sorting of balanced inversion polymorphisms present in the ancestral Mexican/U.S. population. In this scenario, Mexican and Northern isolates diverged recently from a common ancestor of modest population size, accounting for the shallow RNDs for loci mapping to chromosomes 4 and 5. In contrast, rearranged regions on chromosomes 1-3 tend to have deeper RNDs because of (i) limited recombination between inversion karyotypes (Mexican and U.S. haplotypes on alternate inversions may often be restricted from coalescing until before the origin of the chromosomal rearrangement separating them in the common ancestor) and (ii) the increased retention time of rearrangements in the ancestral population due to overdominance. At the time of population subdivision, the inversions may have been arrayed in the form of primary clines. Inversions prominent in the South consequently sorted into the Mexican fly population, while a large portion of the polymorphism was retained in the North. As a result, SN haplotypes (alleles that now vary clinally and are found in increasing frequency in southern U.S. fly populations) are genetically more closely related to M haplotypes in Mexico than to alternate N haplotypes segregating in the same host populations ( Fig. 2 A and supporting information).

However, in the absence of a mechanism that coordinately generates inversions throughout the genome, the incomplete lineage-sorting hypothesis has difficulty explaining the clustered distribution of RND values for chromosome 1-3 loci into intermediate and deep categories ( Fig. 3 ). Correlated RND values may be expected among loci residing in the same inverted region of a chromosome but not among rearranged regions on different chromosomes, as noted. Moreover, incomplete lineage sorting cannot readily account for the deep RND seen for mtDNA and its congruence with many chromosome 1-3 loci (Figs. ​ (Figs.2 2 and ​ and3 3 and Table 1 ). Given a recent time of separation and modest effective size for the ancestral population, mtDNA should have coalesced quickly and should display minimal differentiation between Mexican and U.S. flies. Last, although inverted regions can be biased toward containing haplotypes with deeper RNDs, unless population splitting was precise, one would still expect to see a subset of inversions shared in common between Mexican and U.S. flies. Haplotypes in the shared inversions should show shallow RNDs, similar to loci on chromosomes 4 and 5. Consequently, the observed gene trees are more consistent with the hypothesis of repeated isolation and secondary contact, with inversions on chromosomes 1-3 becoming increasing more recalcitrant to introgression through time relative to collinear regions of the genome.

Our data could also be explained by a series of gene duplication and deletion events within R. pomonella and the outgroup species R. electromorpha such that many of the haplotype comparisons made in the study were between paralogous rather than orthologous sequences. Four of the original 19 loci amplified in the study were found to be duplicate loci. If similar duplications were accompanied by deletions for many of the other 15 loci, then these duplications/deletions could confound our biogeographic interpretation of the gene trees. However, the deletion scenario, considered alone, suffers the same difficulties as the lineage-sorting hypotheses in explaining the tripartite distribution and deep congruence of chromosome 1-3 nuclear and mtDNA RND values. But it is possible that a composite biogeography/deletion model could account for the pattern. Under this scenario, Mexican and Northern isolates formed 𢒁.57 Mya. A period of secondary contact and gene flow followed from 0.5-1 Mya. After this time, Altiplano and Northern populations have remained disjunct. The shallow RNDS observed for loci not on chromosomes 1-3 would be due reciprocal deletions of paralogous genes in R. pomonella and R. electromorpha, resulting in improper comparisons of orthologous Mexican and U.S. haplotypes within R. pomonella to a highly diverged paralogous outgroup sequence for R. electromorpha.

The deletion hypothesis would not negate the contributory roles of allopatry and secondary introgression in facilitating the sympatric radiation of the R. pomonella group by means of host shifting. However, it would call into question whether gene flow was differential for inverted vs. collinear regions of the genome. In essence, there would not have been a second period of recent contact when such a pattern could have been fully generated. Genetic crosses of flies imply that U.S. haplotypes represent allelic variation segregating at single loci (30, 35). However, it is difficult to completely rule out the possibility that deletions at very tightly linked duplicated loci generated the observed segregation patterns. Moreover, test cross results for R. pomonella are not directly germane to resolving the status of R. electromorpha sequences. However, sequence data available for the more distantly related R. cingulata and R. suavis for P661, P309, P2620, and P3060 (loci with shallow RNDs) place R. electromorpha between these two species and R. pomonella. The lack of interspersed clades of sequences containing all or subsets of the four species implies that variation at P661, P309, P2620, and P3060 is allelic and not paralogous.

A Second Mexican Population. Recently, we have discovered a second population of R. pomonella-like flies that infest hawthorns in the Sierra Madre Oriental mountains of Mexico ( Fig. 1 ). The genetics, biogeography, and phenology of the Sierra Oriental population suggest that it may have been a conduit for gene flow between the Altiplano and the North in the past (J.R., J.L.F., X.X., S. Berlocher, and M.A., unpublished data). DNA sequence analysis indicates that Sierra flies are differentiated but, overall, appear to be most closely related to southern U.S. populations (X.X. and J.L.F., unpublished data). The Sierra population abuts the Altiplano population through parts of the states of Veracruz, Puebla, and Hidalgo, Mexico ( Fig. 1 ) (J.R., J.L.F., X.X., S. Berlocher, and M.A., unpublished data). We do not know whether the Sierra population contacts U.S. flies. However, if it does, this contact zone is spotty and ephemeral. Hawthorns are rare through the border region but are present in isolated patches in southern New Mexico and, possibly, the Davis Mountains of Texas. The primary hawthorn host for Sierra flies is C. rosei var. parrayana, which is infested from September to early October (J.R., J.L.F., S. Berlocher, and M.A., unpublished data). As is the case for Altiplano and U.S. flies, the diapause characteristics of the Sierra population match host phenology. Sierra flies eclose significantly earlier than Altiplano flies, resulting in potentially substantial allochronic isolation (J.R., J.L.F., X.X., S. Berlocher, and M.A., unpublished data). However, host specificity is not absolute in Mexico. In the transition region between the Altiplano and Sierra, C. mexicana and C. rosei rosei cooccur with C. rosei parrayana and can be found infested by genetically Sierra populations of flies. Here, C. mexicana and C. rosei rosei fruit earlier than they do on the Altiplano and are infested from late September to early November. Thus, host specificity is not as critical a factor isolating Mexican flies as it is for the R. pomonella complex in the United States. However, the spatial and temporal overlap of hawthorns in the transition zone provides a potential bridge for past introgression between the Altiplano and North via the Sierra population.

A Golden Braid. The views of Mayr, Dobzhansky, and Bush may not be as trichotomous as they seem with respect to Rhagoletis. Geographic isolation appears to have established an initial kernel of genetic differentiation that was later expanded on and contributed to sympatric host shifts and new fly taxa. Thus, although geographic context is critical for understanding speciation, allopatry and sympatry should not always be considered as diametrically opposed modes of divergence along an axis of spatial isolation. Differentiation and processes occurring in isolation and contact can interact and compliment each other to accentuate species formation, arguing for a more pluralistic view of modes of speciation (40). In the case of R. pomonella, the relationship involves a likely sequence of geographic isolation, life-history adaptation, secondary contact, differential introgression, inversion clines, and sympatric host shifts. The evolution of reinforcement can be viewed in an analogous manner, involving non-host-related traits affecting prezygotic isolation rather than ecological adaptation per se. Also, there is no reason to presume that host-related differences that originated in sympatry cannot be solidified by periods of geographic isolation between host-associated populations, although such allopatry is not required to complete the speciation process. Thus, during the time course of differentiation, populations can assume characteristics of both allopatric and sympatric modes of divergence, with phenotypic and genetic elements interacting to further the speciation process.

The connectivity of speciation mode is perhaps best epitomized for R. pomonella if one views the phylogeography of the fly as reflecting sequential adaptation to spatially more finely packaged phenological host niches. At the coarsest level, Altiplano, Sierra Oriental, and Northern R. pomonella populations initially became differentially adapted to temporal and spatial disjunctions in hawthorn fruiting time through a “modular” genetics associated with inversions affecting diapause. After secondary introgression from Mexico, the modular gene blocks became arrayed in the form of broad inversion clines in the North in response to latitudinal variation in hawthorn fruiting time. Last, life-history variation inherent in the clines was extracted on a microgeographic scale [primarily by shifts in allele (inversion) frequencies] to facilitate sympatric shifts and specialization of R. pomonella in the United States to a number of cooccurring host plant species with differing fruiting times. However, host specificity does not appear to be a factor reproductively isolating Altiplano and Sierra flies. Here, geography may act as habitat fidelity does in sympatry, limiting migration and facilitating divergence.

Materials and Methods

Phylogenetic Tree and Population Structure Analyses.

A total of 1,364,793 SNPs in coding regions (exonic and intronic) were used for population genetics analysis. To clarify the phylogenetic relationships from a genome-wide perspective, an individual-based neighbor-joining tree was constructed using the p-distance as implemented in TreeBeST (v1.9.2), with bootstrap values determined from 1,000 replicates (38). The population genetic structure was examined using the program ADMIXTURE (v1.23) (39). A total of 35 accessions were used to estimate the genetic ancestry, specifying a K ranging from 2 to 3. A principal component analysis was also conducted to evaluate the genetic structure of the populations using GCTA (40). First, a genetic relationship matrix was obtained using the parameter “–make-grm” then, the top three principal components were estimated with “–pca3”.

Detection of Gene Flow Using TreeMix.

Population relatedness and migration events were inferred using TreeMix (41). The 1,364,793 coding-region SNPs were used to build a maximum-likelihood tree, with a window size of 2,000 SNPs. This was repeated 10 times. The tree with the lowest SE for the residuals was selected as the base tree topology. The population pairs with an above-zero standard residual error were identified as candidates for admixture events, representing populations that the data indicate are more closely related to each other than is demonstrated in the best-fit tree (41). TreeMix was then run using between one and six introduced migration events. When three migration events were added, the residuals were much lower than for the trees generated using other numbers of migration events.

PSMC Analysis.

PSMC was used to analyze the evolutionary demographic changes of wild emmer wheat in “Evolution Canyon” (Mt. Carmel, Israel). We selected three samples from each population with the highest depth to represent each population. Genotype calls for each position were made using the SAMtools (v1.19) mpileup command, filtering for reads with minimum base and mapping quality scores of 30. Occasional heterozygous sites were dealt with by randomly sampling one allele. Population divergence time and effective population sizes were estimated by PSMC with a mutation rate of 6.5 × 10 −9 substitutions per site per year and a generation time of one generation per year.

Genome-Wide Selective Sweep Analysis.

In order to identify selective sweeps in the SFS1 population, we combined irradiance-intolerant populations (SFS1 and NFS) in a single group to exclude the potential effect of genetic drift. We used a likelihood method (the cross-population composite likelihood ratio, XP-CLR) with the following parameter: –w1 0.02 200 10000 –p0 0.95. To run XP-CLR, we assigned all SNPs to genetic positions based on 0.18 cM/Mb for the A and B subgenomes (26). Windows with the top 5% XP-CLR values were identified. For candidate genes, Gene Ontology (GO) enrichment analysis was performed using the R program with the default parameters (P < 0.05 and FDR < 0.05).

Cytogenetic Analysis.

Seeds were germinated on moist filter paper in the dark at room temperature until the roots grew to 1.5 to 2.0 cm in length. The excised root tips were then treated as described before (42). The synthesized oligonucleotide probes Oligo-pSc119.2, Oligo-pTa535, and Oligo-(GAA)7 (Invitrogen Biotechnology) were 5′ end-labeled with 6-carboxyfluorescein (6-FAM) for green or 6-carboxytetramethylrhodamine (Tamra) for red signals. Probe Oligo-3A1 (FAM-5′-AATAATTTTACACTAGAGTTGAACTAGCTCTATAAGCTAGTTCA-3′) was used to distinguish signal size and location differences in chromosomes 3A and 7A. The probe solution (20 ng/μL in 2× SSC and 1× TE buffer, pH 7.0) was denatured for 5 min in boiling water and then placed on ice. A 6-μL probe solution was used for each slide. The hybridization was performed at 37 °C overnight in a humid chamber. After hybridization, the slides were washed using 2× SSC and then mounted with a Vectashield mounting medium containing 1.5 μg/mL 4,6-diamidino-2-phenylindole (DAPI Vector Laboratories). Images were captured with an Olympus BX-51 microscope equipped with a DP-70 CCD camera. Particular chromosomes were identified by comparing the signal pattern of probes hybridized to hexaploid wheat according to ref. 22.

Data and Material Availability.

The resequencing and SNP data generated in this work are deposited in the Genome Sequence Archive in the BIG Data Center, Beijing Institute of Genomics, Chinese Academy of Sciences, under the accession no. CRA001873.

Convergent character displacement in sympatric tamarin calls (Saguinus spp.)

Character displacement, or a shift in traits where species co-occur, is one of the most common ecological patterns to result from interactions between closely related species. Usually, character displacement is associated to divergence in traits, though, they might be convergent, especially when used for aggressive interference between species. In the context of animal communication, territorial calls are predicted to converge in order to increase context recognition and decrease the costs of ecological interference competition. However, such signals might also be adapted to characteristics of the shared environment. In this study, we used data from 15 groups of two parapatric tamarins, Saguinus midas and S. bicolor, to test for similarities in long calls among sympatric and allopatric groups. We hypothesized that calls would converge in sympatric areas, as it would be mutually beneficial if both species recognize territorial contexts, but that convergence would depend on forest type due to acoustic adaptation. As predicted, long calls converged in sympatry, with S. midas shifting its calls towards S. bicolor’s acoustic pattern. However, this shift only occurred in primary forest. In sympatric areas, S. midas produced sounds with narrower bandwidths in primary than in secondary forest, consistent with optimization of sound propagation while both species produced longer calls in primary forests independently of geographic location (i.e. sympatry and allopatry). Our results suggest that both social and environmental pressures are important in shaping tamarin sounds. As their effects can interact, analyses, which assume that these ecological pressures act independently, are likely to miss important patterns.

Significance statement

Territorial signals between closely related sympatric species are expected to be convergent to increase context recognition and decrease the costs of interference competition. However, such signals might also be adapted to characteristics of the shared environment, such as forest structure characteristics. We analysed vocalisations from two parapatric tamarins and found that, though their long calls asymmetrically converged in sympatry, only red-handed tamarins shifted towards pied tamarin call type, and this only occurred in primary forest. Our results suggest that both social and environmental pressures are important in shaping primate calls. Because their effects can interact, analyses which assume that these pressures act independently, are likely to miss important patterns.

The Role of Sympatric and Allopatric Speciation in the Origin of Biodiversity of Herbivorous Insects, with Palaearctic Species of the Genus Macropsis Lewis, 1836 Taken as an Example (Homoptera, Auchenorrhyncha, Cicadellidae, Eurymelinae, Macropsini)

Using 60 Palaearctic species of the leafhopper genus Macropsis as an example, the contribution of sympatric and allopatric speciation to the origin of herbivorous insect biodiversity was studied. According to the previously reconstructed evolutionary scenarios, in the temperate zone of the Palaearctic Region the genus Macropsis probably dispersed from east to west and formed 10 natural groups, with species within each group being similar both in morphological traits and in host specialization. The hypothetical speciation modes for each group can be largely inferred from geography. If related species replace each other in different zoogeographic regions, they are likely to have arisen as the result of allopatric speciation. If the species show overlapping distributions and live on the same host plant, they must have originated in allopatry and become secondarily sympatric due to subsequent dispersal. Finally, if related species have strongly overlapping ranges and populate similar habitats but differ in host specializations, this may indicate their origin as the result of sympatric speciation due to host plant shifts. For 31 species (51.7%), allopatric speciation seems to be the most likely or even the only possible scenario, whereas for 20 species (33.3%), the hypothesis of sympatric speciation is either convincingly substantiated or at least quite feasible. The origins of the remaining 9 species (15%) remain unknown. Therefore, sympatric speciation is not a rare phenomenon in Macropsis, but it certainly does not predominate over the allopatric mode. Thus, even within the same genus of herbivorous insects, speciation can occur in different ways: in the allopatric mode, when a host plant shift is possible but not essential, and in the sympatric mode, when divergence is triggered by the host shift. Cases of intraspecific differentiation, which can be considered as initial stages of speciation, are also discussed. These are allopatric color forms associated with the same host plant, allopatric color forms associated with different plants and, finally, forms living on different sympatric or allopatric hosts but showing no difference in coloration. It is shown that divergence is not always caused by transition to a new host plant even in specialized herbivores.


Since its inception, the field of speciation research has been marked by spirited debate. Even fundamental problems such as how reproductive barriers evolve and which barriers contribute to speciation have not yet been resolved. There is continued interest in settling these persistent controversies. For example, recent proposals to distinguish ecological from nonecological speciation ( Schluter 2001 Rundle and Nosil 2005 Schluter 2009 ) have brought greater attention to the role of ecology and natural selection in the evolution of reproductive isolating barriers. Yet, since Darwin, ecology has always been acknowledged as a major factor in speciation ( Dobzhansky 1937 Stebbins 1950 Mayr 1947 Dobzhansky 1951 Mayr 1963 Schemske 2000 Coyne and Orr 2004 ). Of the three purported categories of nonecological speciation ( Schluter 2001 ), only genetic drift is unambiguously nonecological, but it is probably too slow to cause speciation without some ecological adaptation occurring along the way. Hence, speciation purely by genetic drift is probably rare. Of the remaining categories of putative nonecological speciation, speciation by uniform selection and by polyploidy virtually always involve ecological factors. Ecology is so intertwined with the evolution of reproductive isolation during adaptive divergence that we question whether “pure” nonecological speciation ever occurs in nature. Hence, we suggest that the recently proposed dichotomy between ecological and nonecological speciation is both flawed and unnecessary.

The longstanding view that speciation mechanisms can be studied only in sympatric populations has led to the virtual neglect of geographic isolation as a legitimate isolating barrier. We argue that a genetically based difference in the geographic ranges of populations and species due to local adaptation is an important and overlooked isolating barrier. This ecogeographic isolation can be distinguished from the effective geographic isolation, which can include contributions from historical and genetic factors, through reciprocal transplant experiments and/or ecological niche modeling. Although these approaches are often difficult to implement, they are necessary to evaluate how genetically based differences in the spatial distributions of populations and species may have contributed to speciation, and how current and future distributions might affect gene flow.

One of the major goals of speciation research is to identify the relative contributions of relevant isolating barriers between recently diverged species. This requires (1) estimating the strength of all potential isolating barriers, (2) evaluating the time course for the evolution of barrier strengths, and (3) determining how each potential barrier contributes to the total isolation. In terms of the order of appearance in the life history, the isolating barriers that first come into play are of particular significance as subsequent barriers can only stop gene flow that remains after the effects of earlier-acting barriers. In this regard, ecogeographic isolation is often the first potential barrier to operate, and thus must be considered in any comprehensive study. Failure to include early-acting barriers, may lead to an overemphasis on the importance ascribed to barriers such as gametic isolation and intrinsic genetic incompatibilities that can only operate in sympatry.

We therefore suggest that it is useful to distinguish barriers that actually reduce gene flow under current conditions from those for which a reduction in gene flow is expected only if the geographic distribution of species or populations changes. For example, local adaptation leading to habitat isolation should generally be regarded as realized isolation whereas hybrid sterility is a potential barrier for allopatric populations but can become realized if populations become sympatric. Making the distinction between realized and potential isolating barriers and identifying their rates of evolution is critical for distinguishing barriers that contribute to speciation from those that evolve after speciation is complete.

We see the following as fertile opportunities for improving our understanding of speciation:

Estimate the strength of ecogeographic isolation. Although some studies have examined effective geographic isolation between taxa, few have added information that allows for the assessment of ecogeographic isolation (e.g., Angert and Schemske 2005 ). In many systems, potentially important barriers such as mating discrimination and intrinsic postzygotic isolation have been measured without parallel information on ecogeographic isolation. Adding this component of isolation will allow a more accurate assessment of realized barrier strengths.

Estimate the components of reproductive isolation between sister species and assess the rate of evolution of different reproductive barriers. Because reproductive isolation accumulates after speciation is complete, studies of taxa that have only recently become species are particularly informative (e.g., Ramsey et al. 2003 Kay 2006 Martin and Willis 2007 ). Furthermore, comparative studies of multiple pairs of sister species are needed to determine if there are general patterns, e.g., which barriers evolve first? This question can be addressed in part by estimating the relationship between genetic distance and the magnitude of reproductive isolation for individual barriers, such as the classic studies of Coyne and Orr (1989, 1997) . When such data are compared to estimates of contemporary barrier strength, it will be possible to assess which barriers are most “important” in speciation.

Consider the distinction between ephemeral and permanent reproductive barriers. Although the linear sequential model provides guidance for evaluating the importance of contemporary barriers, later acting barriers may deserve attention due to their increased potential for permanence.

Identify the traits involved in speciation. Few studies have investigated both the isolating barriers important in speciation and the traits responsible for those barriers (e.g., McKinnon et al. 2004 Bradshaw and Schemske 2003 ).

Assess how adaptation contributed to the evolution of traits conferring reproductive isolation. Although it seems clear that adaptation is a key feature of speciation, few studies have identified the link between natural selection and adaptive traits that directly or indirectly cause reproductive isolation. The use of segregating hybrid populations ( Schemske and Bradshaw 1999 ) and/or allele substitution lines ( Bradshaw and Schemske 2003 ) can help reconstruct the selective scenarios that resulted in speciation.

Elucidate the genetic architecture of reproductive isolating barriers. This will require methods such as Quantitative Trait Locus (QTL) mapping for estimating the number, location, magnitude of effect and mode of action of genes and genomic regions that contribute to reproductive isolation (e.g., Bradshaw et al. 1998 Bouck et al. 2007 ). In addition, reverse genetic approaches such as comparative outlier scans applied to hybridizing taxa could be used to distinguish regions of the genome where gene flow is restricted due to local selection (e.g., Egan et al. 2008 Nosil et al. 2008) . These two approaches can be combined to provide additional insight into the interaction between adaptation and the genome ( Via and West 2008 ). We expect that most isolating barriers will result directly or indirectly from the evolution of adaptive traits, but it is also important to characterize neutral or deleterious genes that confer reproductive isolation, as might be expected in some cases of intrinsic postzygotic incompatibilities. Furthermore, although it is well established that through pleiotropy, adaptive mutations can affect multiple ecological traits ( McKay et al. 2003 ), the role of pleiotropy in speciation is largely unstudied. Thus, genetic approaches for comparing direct and indirect contributions to reproductive isolation are of particular interest.

Evaluate the role of chromosomal rearrangements in speciation. Stochastic forces may sometimes interact with adaptive processes to affect the resulting reproductive isolation. Chromosomal inversions, for example, may enhance isolation by building complexes of genes that are protected from recombination (e.g., Brown et al. 2004 ).

We advocate an approach to the study of speciation first envisioned by Dobzhansky and Mayr in which reproductive isolation is the primary focus. Although these early leaders of our field would have almost certainly embraced new molecular and computational approaches for the study of speciation, the conceptual framework they established is still applicable today. We continue to seek answers to fundamental questions such as: Which forms of reproductive isolation are responsible for speciation? What traits and selective forces are involved? and What is the genetic basis of reproductive isolation?

The answers will come from comprehensive studies of populations and species living in sympatry or allopatry, for which we estimate all relevant isolating barriers, whether they are ecological or nonecological or act prior to or after fertilization or hybrid formation. This is consistent with Mayr's view ( Mayr 1947 , p. 278) that “… most isolating mechanisms between closely related species that have been studied thoroughly were found to be multiple. There always seem to be involved (1) differences in the ecological requirements, (2) reduction of the mutual sexual stimulation, and (3) reduction in the number and the viability of the offspring.” We suggest that future progress will be best achieved by embracing this inclusive approach towards understanding the “biology of speciation.”

Associate Editor: M. Rausher


Recent studies have highlighted that novel genomics approaches and genome-wide data can provide new insights into the geographical context and underlying processes of sympatric speciation.

Sympatric speciation is the evolutionary divergence and reproductive isolation of sister species arising from a single ancestral species in the absence of any barriers to gene flow. As such, this apparently rare phenomenon offers important insights into the role of selection in driving speciation.

Genomic studies have reassessed what were thought to be compelling empirical examples of sympatric speciation. In some cases, these studies have found evidence for multiple colonisations and homogenisation of the genomes of the two waves of colonisers upon secondary contact. In other examples, the findings have strengthened the case for divergence in sympatry. Understanding the biogeography and evolutionary history of the genomic regions underlying ecological adaptation and sexual selection is fundamental to understanding how speciation can progress when driven by natural and sexual selection without any period of physical separation.

Sympatric speciation has been of key interest to biologists investigating how natural and sexual selection drive speciation without the confounding variable of geographic isolation. The advent of the genomic era has provided a more nuanced and quantitative understanding of the different and often complex modes of speciation by which sympatric sister taxa arose, and a reassessment of some of the most compelling empirical case studies of sympatric speciation. However, I argue that genomic studies based on contemporary populations may never be able to provide unequivocal evidence of true primary sympatric speciation, and there is a need to incorporate palaeogenomic studies into this field. This inability to robustly distinguish cases of primary and secondary ‘divergence with gene flow’ may be inconsequential, as both are useful for understanding the role of large effect barrier loci in the progression from localised genic isolation to genome-wide reproductive isolation. I argue that they can be of equivalent interest due to shared underlying mechanisms driving divergence and potentially leaving similar patterns of coalescence.

Watch the video: What is HETEROPATRIC SPECIATION? What does HETEROPATRIC SPECIATION mean? (January 2023).