Factors analyzed in ANOVAs to determine if geography can account for variation in the occurrence of reproductive isolation.
Pairwise comparison of Hyalella sequences yielded 97 unique Hyalella haplotypes; three of the populations we sequenced had only one haplotype while the other two had two haplotypes each Table S5.
Appreciable molecular divergence was detected within Hyalella with evidence of saturation Figure 2. To facilitate discussion of the phylogeny, haplotypes are grouped into clades Figure 1 , Table S5. Terminal nodes represent unique haplotypes. Haplotypes were grouped into clades where applicable. Bayesian posterior probabilities are given at all major nodes.
COI saturation plot. The solid line has a slope of 1 and is a theoretical representation of sequence data that would occur if there was no saturation Jeffroy et al. The observed departure from this theoretical slope which occurs at around 0. Populations segregate with some degree of overlap. Phylomorpho plot of population centroids with phylogenetic relationship. Genetic similarity is not related to distribution of centroids in principal components analysis space.
Decimals along branches represent the Bayesian model inferred number of substitutions. After 8 weeks, all conspecific controls had successfully produced offspring while only three of the potential crosses successfully produced offspring Table 6.
Despite amplexus being observed in all treatment groups, none of the heterospecific pairings involving H. This observation is consistent with those two populations being completely isolated reproductively from all other tested populations. Among the replicates that successfully produced offspring, there was noticeable resistance by the heterospecific pairs to mate.
Conspecific control pairs produced offspring as early as 2 weeks into mating trials while none of the successful heterospecific pairs produced offspring until after at least 4 weeks Figure 5. This result is consistent with interfertile heterospecific populations having some degree of prezygotic reproductive isolation. After rearing hybrid offspring to adulthood, all hybrid offspring successfully produced offspring suggesting that hybrids are fertile.
Cumulative proportion of successfully reproducing pairs across time. By the second week, conspecific pairs had produced offspring; however, none of the heterospecific crosses produced offspring until at least 4 weeks had elapsed. Only the heterospecific crosses that successfully produced offspring are depicted. None of the heterospecific pairings including H. However, geography was found to be an important factor Figure 6 as the number of populations of each clade and the length of reach occupied by each population was both found to significantly explain the occurrence of reproductive isolation Figure 6 , Table 7.
Geographic distribution of clades inferred through genetic analysis for which reproductive isolation was assessed. Note that the populations found to be reproductively isolated occur at only a single locality each while the interfertile populations belong to widely distributed clades.
Geography in both size of distribution and number of known localities for each haplotype was found to significantly explain the occurrence of reproductive isolation. Appreciable morphological and molecular differentiation were observed in the five populations of Hyalella in this study Figure 1 , Figure 3.
The molecular analysis suggests that i the five populations in this study along with numerous other nominal Hyalella populations represent a polytomy with deep divergence, and ii H. Based on the depth of molecular divergence between populations, and the paraphyletic distribution of populations conforming to the H. The observation of morphological diversity not conforming to an inferred history of shared common ancestry is not unique to Hyalella Faria et al.
It is likely that differentiation of lab stock occurred via drift or plasticity due to inevitable bottlenecks when establishing populations in captivity, as morphological divergence and local adaptation have been shown to occur rapidly in captivity Fragata et al.
However, differentiation was convergent toward the H. Only some of the populations were found to be interfertile and this did not strongly correlate with history of common ancestry or morphological similarity Figure 4. The three interfertile populations were interfertile with each other in all possible combinations but never produced offspring with either of the reproductively isolated populations.
The two reproductively isolated populations were shown to be completely reproductively isolated from all three of the interfertile populations as well as from each other.
At this time, the mechanism of reproductive isolation is unknown although amplexus was observed in all combinations, suggesting that the mode of reproductive isolation is gametic or postzygotic for the completely reproductively isolated populations, or at least not entirely behavioral. However, all of the heterospecific mating trials showed evidence of reproductive isolation, including interfertile combinations Figure 5.
This finding demonstrates viable hybridization between morphologically distinct populations and presents evidence of behavioral prezygotic reproductive isolation between populations of what were formerly considered populations of the H. Therefore, divergence between populations likely occurred in the absence of gene flow; thus, sympatrically occurring populations likely represent secondary contact.
It is unclear if divergence occurred directionally due to selection or drift during periods of geographic isolation. However, molecular distance did not predict morphology or reproductive isolation, but geographic range size was found to be negatively correlated with interfertility Figure 6 , Table 7. It is remarkable that Hyalella was recovered as a monophyletic taxon as the depth of divergence between different Hyalella lineages is comparable to the depth of divergence observed among the other amphipod families included in our analysis depth of divergence between outgroups in Figure 1 is comparable to the divergence found within Hyalella.
We also only used a single mitochondrial locus because of the abundance of archived COI sequences for amphipods; however, the rate of divergence may be too rapid at the COI locus to properly estimate relationships with such deep divergence Figure 2.
It is possible that divergence between lineages is approaching saturation which appears to have occurred around 0. However, separate analyses looking at each codon position revealed that first and second codon positions account for observed saturation of the COI locus while the third position conforms to the expectations of neutral evolution Figure S2. A comparison of the amount of observed pairwise substitutions indicates that the third codon position is evolving approximately 2.
It is important to point out that the present study recovered fewer haplotypes than previous authors despite sequencing the same locus and using the same sequences published by other authors on GenBank. This is likely due to the trimming of sequences to much fewer base pairs in order to have a complete alignment as different authors amplified different regions of the COI locus.
Therefore, it is likely that variable sites were eliminated that other authors used to identify haplotypes. Presumably, there is strong stabilizing selection within a population to maintain interfertility with other members of the same population. Therefore, it is more likely that genomic changes that lead to barriers to interfertility will be retained in smaller populations. It is also less likely for larger populations to diverge from the reproductive type of ancestral populations if they experience stabilizing selection for interfertility due to lower susceptibility to drift in larger populations.
Therefore, abundant and widespread taxa experiencing stabilizing selection may maintain interfertility with many different lineages, especially other widespread taxa, while local endemics experience drift or divergent selection. The experimental observations presented herein are consistent with this hypothesis, but it requires further investigation.
Identifying divergent loci associated with reproductive isolation could shed light on the factors that contribute to the evolution of reproductive isolation. Worsham involved in research design, field collections, laboratory experiments, molecular phylogeny, statistical analysis, manuscript preparation, and maps.
Julius involved in field collections and laboratory experiments. Nice involved in molecular phylogeny, statistical analysis, and manuscript preparation. Diaz involved in multivariate statistics and maps. Huffman involved in field collections, material support and manuscript preparation. We are deeply grateful to Gary Wellborn for his invaluable contributions.
Without the numerous volunteers that assisted with field collections, especially Helen Wukasch, Stephen Harding, Alex Zalmat, and Duy Le, this project would not have been possible. We would like to thank Mackenzie Barnett for providing access to one of the sampling locations making this research possible.
Fish and Wildlife Service. Geographic isolation facilitates the evolution of reproductive isolation and morphological divergence. Ecol Evol. National Center for Biotechnology Information , U. Journal List Ecol Evol v. Published online Oct McLean L.
Worsham , 1 , 2 Eric P. Julius , 1 Chris C. Nice , 1 Peter H. Diaz , 3 and David G. Huffman 1. Eric P. Chris C. Peter H. Diaz 3 U. David G. Author information Article notes Copyright and License information Disclaimer.
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Associated Data Supplementary Materials. Abstract Geographic isolation is known to contribute to divergent evolution, resulting in unique phenotypes.
Keywords: evolution, geographic isolation, molecular diversity, morphological diversity, reproductive isolation. Table 1 Collection localities and count of dorsal mucronation for each Hyalella population. Detecting the number of clusters of individuals using the software structure: a simulation study. Jombart, T. Discriminant analysis of principal components: a new method for the analysis of genetically structured populations.
BMC Genetics 11, 94 Bioinformatics 24, — Peakall, R. GenAlEx 6. Population genetic software for teaching and research—an update. Bioinformatics 28, — Rosenberg, M. Version 2. Methods Ecol. Busby, J. Margules, C. Hijmans, R. Very high resolution interpolated climate surfaces for global land areas. Smouse, P.
Multiple regression and correlation extensions of the Mantel test of matrix correspondence. Goslee, S. The ecodist package for dissimilarity-based analysis of ecological data. Examining the full effects of landscape heterogeneity on spatial genetic variation: a multiple matrix regression approach for quantifying geographic and ecological isolation.
Evolution 67, — Download references. You can also search for this author in PubMed Google Scholar. Wang and X. Wu and X. This work is licensed under a Creative Commons Attribution 4. Reprints and Permissions. Sci Rep 5, Download citation. Received : 30 March Accepted : 28 September Published : 23 October Anyone you share the following link with will be able to read this content:. Sorry, a shareable link is not currently available for this article. Provided by the Springer Nature SharedIt content-sharing initiative.
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If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate. Advanced search. Skip to main content Thank you for visiting nature. Download PDF. Subjects Evolution Evolutionary ecology. Abstract Understanding how natural processes affect population genetic structures is an important issue in evolutionary biology.
Introduction Understanding how natural processes affect population genetic structures and gene flows is an important issue in evolutionary biology. Results Genetic diversity and population genetic structure The number of alleles NA , the number of effective alleles NEA and the genotype diversity D ranged from 30 to 75, Full size table. Table 2 Pairwise Bruvo distance between 13 Myriophyllum spicatum populations. Figure 1. Full size image. Figure 2. Figure 3. Table 3 Partial Mantel tests of association between genetic distances and geographic distances and the environmental dissimilarity of Myriophyllum spicatum populations in the QTP and YGP and in two study regions respectively.
Genetic diversity and population genetic structure We previously isolated 20 microsatellite loci from M.
Isolation by distance Mantel tests with 10, permutations were used to detect IBD pattern based on matrices of pairwise Bruvo distance and geographic distance among all populations, as implemented in GenAlEx 6. Additional Information How to cite this article : Wu, Z. References Sork, V. Article Google Scholar Bohonak, A.
Article Google Scholar Wang, I. Article Google Scholar Shafer, A. Article Google Scholar Lee, C. Article Google Scholar Barrett, S. Article Google Scholar Zhao, Y. Google Scholar Aiken, S. Article Google Scholar Yu, D. Google Scholar Lacoul, P. Article Google Scholar Viana, D.
Article Google Scholar Suren, A. Article Google Scholar Lacoul, P. Article Google Scholar Olney, P. Article Google Scholar Brochet, A. Article Google Scholar Shi, M. Article Google Scholar Hirao, A. Article Google Scholar Wu, Z. Article Google Scholar Nei, M. Article Google Scholar Bruvo, R. Article Google Scholar Clark, L. Article Google Scholar Dufresne, F.
Article Google Scholar Ortego, J. Article Google Scholar Pritchard, J. Article Google Scholar Jombart, T. Article Google Scholar Busby, J. Article Google Scholar Smouse, P. Article Google Scholar Goslee, S. Article Google Scholar Download references.
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About this article. Cite this article Wu, Z. Copy to clipboard. Comments By submitting a comment you agree to abide by our Terms and Community Guidelines. Publish with us For authors Submit manuscript. Search Search articles by subject, keyword or author. Show results from All journals This journal. Defining speciation. Reproductive isolation. Subscribe to our newsletter. Email Facebook Twitter. More Details Evo Examples Teaching Resources Read about how speciation factored into the history of evolutionary thought.
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