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Geographic Life History Differences Predict Genomic Divergence Better than Mitochondrial Barcodes or Phenotype - PubMed

  • ️Wed Jan 01 2020

Geographic Life History Differences Predict Genomic Divergence Better than Mitochondrial Barcodes or Phenotype

Daniel P Duran et al. Genes (Basel). 2020.

Abstract

Species diversity can be inferred using multiple data types, however, results based on genetic data can be at odds with patterns of phenotypic variation. Tiger beetles of the Cicindelidiapolitula (LeConte, 1875) species complex have been taxonomically problematic due to extreme phenotypic variation within and between populations. To better understand the biology and taxonomy of this group, we used mtDNA genealogies and multilocus nuclear analyses of 34,921 SNPs to elucidate its evolutionary history and evaluate the validity of phenotypically circumscribed species and subspecies. Genetic analyses recovered two divergent species that are also ecologically distinct, based on adult life history. These patterns are incongruous with the phenotypic variation that informed prior taxonomy, and most subspecies were not supported as distinct evolutionary lineages. One of the nominal subspecies was found to be a cryptic species; consequently, we elevate C. p.laetipennis (Horn, 1913) to a full species. Although nuclear and mtDNA datasets recovered broadly similar evolutionary units, mito-nuclear discordance was more common than expected, being observed between nearly all geographically overlapping taxonomic pairs. Additionally, a pattern of 'mitochondrial displacement' was observed, where mitochondria from one species unidirectionally displace others. Overall, we found that geographically associated life history factors better predict genomic divergence than phenotype and mitochondrial genealogies, and consequently taxon identifications based on mtDNA (e.g., DNA barcodes) may be misleading.

Keywords: Cicindelidia politula; cryptic species; molecular systematics; mtDNA; species complex; taxonomy; tiger beetles.

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Conflict of interest statement

The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1

Representative phenotypic variation within Cicindelidia politula. (A) C. p. politula, Texas: Travis Co., (B–F) C. p. petrophila, Guadalupe Mts. National Park (GMNP), (G,H) C. p. barbaraannae, New Mexico: Otero Co., (I) C. p. barbaraannae, Texas: Hudspeth Co., (J,K) C. p. viridimonticola, New Mexico: Eddy Co., (L) C. p. laetipennis, Mexico: Saltillo.

Figure 2
Figure 2

Map of localities for Cicindelidia politula (see Table S1 for data). Classically defined subspecies are as follows, circles = C. p. politula, squares = C. p. barbaraannae, stars = C. p. viridimonticola, diamonds = C. p. petrophila, pentagons = C. p. laetipennis. Black dots indicate sampling localities for genetic data used in the present analyses. Blue-grey localities represent the nominate C. politula clade, recovered in the mtDNA genealogy (Figure 3A,B) and all genomic analyses (Figure 4 and Figure 5). Sky blue localities represent the C. laetipennis (new combination) clade, also recovered in all genetic analyses (Figure 3, Figure 4 and Figure 5). The two clades are ecologically differentiated, with significantly different adult phenologies (Figure 6). Grey map shading indicates topography, with lighter greys indicating higher elevation. All C. politula localities occur from <100 to 1050 m; all C. laetipennis localities occur from 1100 to 2600 m. Localities georeferenced in Google Earth Pro 7.3 and exported to QGIS 2.14 (

http://qgis.osgeo.org

).

Figure 3
Figure 3

Maximum-likelihood mitochondrial phylogenetic tree. The phylogenetic hypothesis was inferred using ~1kb of the mitochondrial gene CO1. Nodal support values are reported for each node as described in the caption panel of the figure. All tips are named according to the taxonomy prior to the publication of this manuscript. Colors correspond to the respective species and subspecies groups.

Figure 4
Figure 4

Maximum likelihood (raxML) tree based on SNP dataset. Representative dorsal habitus for each taxon are shown, (A,B) topology based on 34,414 total loci for 77 individual taxa. Each individual had at least 1000 loci present, (C) topology based on 28,460 total loci for reduced taxon set of 42 individual taxa to address the placement of C. p. laetipennis in the C. politula group. Genomic extraction of 40-year old pinned C. p. laetipennis specimen yielded fewer loci (35 loci) than recently collected material for other C. politula subspecies.

Figure 4
Figure 4

Maximum likelihood (raxML) tree based on SNP dataset. Representative dorsal habitus for each taxon are shown, (A,B) topology based on 34,414 total loci for 77 individual taxa. Each individual had at least 1000 loci present, (C) topology based on 28,460 total loci for reduced taxon set of 42 individual taxa to address the placement of C. p. laetipennis in the C. politula group. Genomic extraction of 40-year old pinned C. p. laetipennis specimen yielded fewer loci (35 loci) than recently collected material for other C. politula subspecies.

Figure 5
Figure 5

Principal component analysis (PCA) of 2228 SNPs. Loci were limited to those found in a minimum of 50% of individuals in each taxonomic group and in 75% of individuals overall to produce a SNP matrix with relatively little missing data (13.10%). Transparent points represent replicate analyses (N = 25) while opaque points represent the centroids of these replicates.

Figure 6
Figure 6

STRUCTURE analyses of 2228 RADseq loci. Loci were limited to those found in a minimum of 50% of individuals in each taxonomic group and in 75% of individuals overall to produce a SNP matrix with relatively little missing data (12.81%). Delta-K and mean log probability plots are illustrated in Figure S2.

Figure 7
Figure 7

Phenological differentiation between the ‘C. laetipennis clade’ (C. p. laetipennis, C. p. barbaraannae, C. p. petrophila, and C. p. viridimonticola) and C. p. politula. Adult activity data was obtained through published records [21,22,23,24,26,27], museum specimen label data, and the authors field work. (See Table S1). Label dates were converted to Julian date and differences illustrated with boxplots by taxonomic group showing the median, 25th and 75th percentiles, and the 95% confidential intervals displayed. The dots outside of the boxes are outliers.

Figure 8
Figure 8

Discovery of putative hybridization in the phenotypes of wild specimens. Top row: C. politula (left), C. schauppii (right), apparent hybrids and/or backcrosses (middle three). Bottom row: C. laetipennis, stat. nov. (left), C. sedecimpunctata (right), apparent hybrids and/or backcrosses (middle three). Hybrids of both species pairs are intermediate with respect to multiple morphological characters (i.e., chaetotaxy, maculations). Mitochondrial genealogy revealed that introgression was occurring between each of these species pairs where they are in geographic contact (Figure 3).

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