Abstract
Morphologically variable species complexes can present significant challenges to conservation when taxonomic boundaries, and therefore conservation units, are ambiguous. In such cases, the definition of Evolutionarily Significant Units (ESUs) based on high-resolution genomic data can be an effective method to clarify genetic divergence and inform conservation actions. Here, we employ a population genomic approach using SNP data to delineate conservation units in a morphologically ambiguous plant species complex (Conospermum caeruleum; Proteaceae) from a global biodiversity hotspot. Over 200 individuals representing five subspecies and three informal morphological forms were sampled across a wide geographic range. Phylogenomic (ML tree and SplitsTree network) and population genomic (STRUCTURE, PCoA, FST) analyses resolved three divergent genetic groups that were incongruent with the current taxonomy, but consistent with geographic distribution. One ESU was comprised of three genetic subgroups, and these can be considered Management Units (MUs) to conserve population genetic structure and diversity. These MUs were surprisingly incongruent with the current subspecies-level taxonomy, but one MU was consistent with a recently documented morphological form, and all were consistent with ecogeographic distribution. We recommend a full taxonomic revision of the Conospermum genus based on a phylogenomic approach to assess any wider incongruence with morphology, and that conservation strategies should be informed by genetic data. Our study exemplifies the application of genomics to the conservation of a morphologically ambiguous species complex, enabling and enhancing the practical conservation of appropriate units of biodiversity.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahrens CW, Supple MA, Aitken NC et al (2017) Genomic diversity guides conservation strategies among rare terrestrial orchid species when taxonomy remains uncertain. Ann Bot 119:1267–1277. https://doi.org/10.1093/aob/mcx022
Allendorf FW, Funk WC, Aitken SN et al (2022) Conservation and the genomics of populations, third edit. Oxford University Press, Oxford, United Kingdom
Baumsteiger J, Moyle PB, Aguilar A et al (2017) Genomics clarifies taxonomic boundaries in a difficult species complex. PLoS ONE 12:e0189417. https://doi.org/10.1371/journal.pone.0189417
Bennett E (2019) Distribution of Conospermum caeruleum subsp. Busselton
Bennett EM (1995) Conospermum. In: McCarthy PM (ed) Flora of Australia, vol 16. Australian Biological Resources Study, Department of Agriculture, Water and the Environment, Canberra, Australia, pp 224–271
Bickford D, Lohman DJ, Sodhi NS et al (2007) Cryptic species as a window on diversity and conservation. Trends Ecol Evol 22:148–155. https://doi.org/10.1016/j.tree.2006.11.004
Binks RM, Byrne M (2022) Species delimitation, hybridization and possible apomixis in a rapid radiation of western australian Leptospermum (Myrtaceae). Bot J Linn Soc. https://doi.org/10.1093/botlinnean/boac022
Binks RM, Steane DA, Byrne M (2021) Genomic divergence in sympatry indicates strong reproductive barriers and cryptic species within Eucalyptus salubris. Ecol Evol 00:1–15
Binks RM, Wilkins CF, Markey AS et al (2020) Genomic data and morphological re-assessment reveals synonymy and hybridisation among Seringia taxa (Lasiopetaleae, Malvaceae) in remote north-western Australia. Taxon 69:307–320. https://doi.org/10.1002/tax.12233
Bradbury D, Binks RM, Byrne M (2021) Genomic data inform conservation of rare tree species: clonality, diversity and hybridity in Eucalyptus series in a global biodiversity hotspot. Biodivers Conserv 30:619–641. https://doi.org/10.1007/s10531-020-02106-2
Butcher R, Thiele KR (2014) An investigation of taxon boundaries in rare and range-restricted Synaphea (Proteaceae: Conosperminae) species from south-west western Australia. Aust Syst Bot 27:119–144. https://doi.org/10.1071/SB14015
Bylsma R, Walkup DK, Hibbitts TJ et al (2022) Population genetic and genomic analyses of western Massasauga (Sistrurus tergeminus ssp.): implications for subspecies delimitation and conservation.Conserv Genet23
Byrne M, Koenders A, Rogerson K et al (2016) Genetic and morphological analysis of multi-stemmed plants of tuart (Eucalyptus gomphocephala). Aust J Bot 64:704–714. https://doi.org/10.1071/BT16091
Calevo J, Gargiulo R, Bersweden L et al (2021) Molecular evidence of species- and subspecies-level distinctions in the rare Orchis patens s.l and implications for conservation. Biodivers Conserv 30:1293–1314. https://doi.org/10.1007/s10531-021-02142-6
Chalcoff VR, Ezcurra C, Aizen MA (2008) Uncoupled geographical variation between leaves and flowers in a South-Andean Proteaceae. Ann Bot 102:79–91. https://doi.org/10.1093/aob/mcn057
Close DC, Messina G, Krauss SL et al (2006) Conservation biology of the rare species Conospermum undulatum and Macarthuria keigheryi in an urban bushland remnant. Aust J Bot 54:583–593. https://doi.org/10.1071/BT05205
Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing with the species-population continuum in the age of genomics. Front Ecol Evol 6:1–13. https://doi.org/10.3389/fevo.2018.00165
Crisp MD, Weston PH (1993) Geographic and ontogenetic variation in morphology of australian waratahs (Telopea: Proteaceae). Syst Biol 42:49–76
Cruz VMV, Kilian A, Dierig DA (2013) Development of DArT marker platforms and genetic diversity assessment of the U.S. collection of the new oilseed crop Lesquerella and related species. PLoS ONE 8:1–13. https://doi.org/10.1371/journal.pone.0064062
De Queiroz K (2020) An updated concept of subspecies resolves a dispute about the taxonomy of incompletely separated lineages. Herpetol Rev 51:459–461
Delnevo N, Piotti A, Carbognani M et al (2021) Genetic and ecological consequences of recent habitat fragmentation in a narrow endemic plant species within an urban context. Biodivers Conserv. https://doi.org/10.1007/s10531-021-02256-x
Delnevo N, van Etten EJ, Byrne M, Stock WD (2019) Floral display and habitat fragmentation: Effects on the reproductive success of the threatened mass - flowering Conospermum undulatum (Proteaceae). Ecol Evol 1–10. https://doi.org/10.1002/ece3.5653
Delnevo N, van Etten EJ, Clemente N et al (2020) Pollen adaptation to ant pollination - a case study from the Proteaceae. Ann Bot 126:377–386
Fišer C, Robinson CT, Malard F (2018) Cryptic species as a window into the paradigm shift of the species concept. Mol Ecol 27:613–635. https://doi.org/10.1111/mec.14486
Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496. https://doi.org/10.1016/j.tree.2012.05.012
Garner BA, Hand BK, Amish SJ et al (2016) Genomics in conservation: case studies and bridging the gap between data and application. Trends Ecol Evol 31:81–82. https://doi.org/10.1016/j.tree.2015.10.009
Georges A, Gruber B, Pauly GB et al (2018) Genomewide SNP markers breathe new life into phylogeography and species delimitation for the problematic short-necked turtles (Chelidae: Emydura) of eastern Australia. Mol Ecol 27:5195–5213. https://doi.org/10.1111/mec.14925
Ghisbain G, Lozier JD, Rahman SR et al (2020) Substantial genetic divergence and lack of recent gene flow support cryptic speciation in a colour polymorphic bumble bee (Bombus bifarius) species complex. Syst Entomol 45:635–652. https://doi.org/10.1111/syen.12419
Gosper CR, Hopley T, Byrne M et al (2019) Phylogenomics shows lignotuber state is taxonomically informative in closely related eucalypts. Mol Phylogenet Evol 135:236–248. https://doi.org/10.1016/j.ympev.2019.03.016
Gruber B, Unmack PJ, Berry OF, Georges A (2018) DARTR: an R package to facilitate analysis of SNP data generated from reduced representation genome sequencing. Mol Ecol Resour 18:691–699. https://doi.org/10.1111/1755-0998.12745
Hoang DT, Chernomor O, Von Haeseler A et al (2018) UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol 35:518–522. https://doi.org/10.1093/molbev/msx281
Hohenlohe PA, Funk WC, Rajora OP (2021) Population genomics for wildlife conservation and management. Mol Ecol 30:62–82. https://doi.org/10.1111/mec.15720
Hosegood J, Humble E, Ogden R et al (2020) Phylogenomics and species delimitation for effective conservation of manta and devil rays. Mol Ecol 29:4783–4796. https://doi.org/10.1111/mec.15683
Houston TF (1989) Leioproctus bees associated with western australian smoke bushes (< i?Conospermum spp.) and their adaptions for foraging and concealment (Hymenoptera: Colletidae: Paracolletini). Rec ofthe West Aust Museum 14:275–292
Huang G, Rymer PD, Duan H et al (2015) Elevated temperature is more effective than elevated [CO2] in exposing genotypic variation in Telopea speciosissima growth plasticity: implications for woody plant populations under climate change. Glob Chang Biol 21:3800–3813
Huson DH, Bryant D (2006) Application of phylogenetic networks in evolutionary studies. Mol Biol Evol 23:254–267. https://doi.org/10.1093/molbev/msj030
Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806. https://doi.org/10.1093/bioinformatics/btm233
Jombart T (2008) Adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405
Kalyaanamoorthy S, Minh BQ, Wong TK et al (2017) ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods 14:587–589
Kilian A, Wenzl P, Huttner E et al (2012) Diversity arrays technology: a generic genome profiling technology on open platforms. Methods Mol Biol 888:67–89. https://doi.org/10.1007/978-1-61779-870-2_5
Ladd PG, Bowen BJ (2020) Pollen release in the Proteaceae. Plant Syst Evol 306. https://doi.org/10.1007/s00606-020-01707-2
Mace GM (2004) The role of taxonomy in species conservation. Philos Trans R Soc B Biol Sci 359:711–719. https://doi.org/10.1098/rstb.2003.1454
Marchese C (2015) Biodiversity hotspots: a shortcut for a more complicated concept. Glob Ecol Conserv 3:297–309. https://doi.org/10.1016/j.gecco.2014.12.008
Menz MHM, Phillips RD, Anthony JM et al (2015) Ecological and genetic evidence for cryptic ecotypes in a rare sexually deceptive orchid, Drakaea elastica. Bot J Linn Soc 177:124–140
Minh BQ, Nguyen MAT, Von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195. https://doi.org/10.1093/molbev/mst024
Moritz C (1994) Defining “Evolutionarily significant Units” for conservation. Trends Ecol Evol 9:373–375. https://doi.org/10.1016/0169-5347(94)90057-4
Myers N, Mittermeier RA, Mittermeier CG et al (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274. https://doi.org/10.1093/molbev/msu300
O’Brien D, Laikre L, Hoban S et al (2022) Bringing together approaches to reporting on within species genetic diversity. J Appl Ecol 59:2227–2233. https://doi.org/10.1111/1365-2664.14225
Oksanen J, Blanchet FG, Friendly M et al (2020) vegan: Community Ecology package. R package version 2.5-7
Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28:2537–2539
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Rambaut A (2018) FigTree v 1.4.2. http://tree.bio.ed.ac.uk/software/figtree/
Ramsay HP (1963) Chromosome numbers in the proteaceae. Aust J Bot 11:1–20. https://doi.org/10.1071/BT9630001
Rossetto M, Yap JYS, Lemmon J et al (2021) A conservation genomics workflow to guide practical management actions. Glob Ecol Conserv 26:e01492. https://doi.org/10.1016/j.gecco.2021.e01492
Rubinoff D, Reil JB, Osborne KH et al (2020) Phylogenomics reveals conservation challenges and opportunities for cryptic endangered species in a rapidly disappearing desert ecosystem. Biodivers Conserv 29:2185–2200. https://doi.org/10.1007/s10531-020-01968-w
Sansaloni CP, Petroli CD, Carling J et al (2010) A high-density diversity arrays technology (DArT) microarray for genome-wide genotyping in Eucalyptus. Plant Methods 6:1–11. https://doi.org/10.1186/1746-4811-6-16
Schmidt H, Trifinopoulos J, Bui M (2021a) Frequently asked questions. http://www.iqtree.org/doc/Frequently-Asked-Questions#how-do-i-interpret-ultrafast-bootstrap-ufboot-support-values. Accessed 9 May 2022
Schneider HM (2022) Characterization, costs, cues and future perspectives of phenotypic plasticity.Ann Bot1–18
Schweizer RM, Saarman N, Ramstad KM et al (2021) Big data in conservation genomics: boosting skills, hedging bets, and staying current in the field. J Hered 112:313–327. https://doi.org/10.1093/jhered/esab019
Sinclair E, Cheetham B, Krauss S, Hobbs R (2008) Morphological and molecular variation in Conospermum triplinervium (Proteaceae), the tree smokebush: implications for bushland restoration. Aust J Bot 56:451–460. https://doi.org/10.1071/BT07137
Stace HM, Douglas AW, Sampson JF (1998) Did “paleo-polyploidy” really occur in Proteaceae? Aust Syst Bot 11:613–629
Stone LM (2003) Floral biology and propagation of blue-flowered Conospermum spp. PhD Thesis, Murdoch University
Stone LM, Seaton KA, Byrne M, Mccomb JA (2006) A study of the reproductive biology of blue-flowered Conospermum species (Proteaceae). Aust J Bot 54:543–551. https://doi.org/10.1071/BT05125
Strand JA, Weisner SEB (2004) Phenotypic plasticity - contrasting species-specific traits induced by identical environmental constraints. New Phytol 163:449–451
Stronen AV, Norman AJ, Vander Wal E, Paquet PC (2022) The relevance of genetic structure in ecotype designation and conservation management. Evol Appl 15:185–202. https://doi.org/10.1111/eva.13339
Supple MA, Shapiro B (2018) Conservation of biodiversity in the genomics era. Genome Biol 19:1–12. https://doi.org/10.1186/s13059-018-1520-3
Tonzo V, Papadopoulou A, Ortego J (2019) Genomic data reveal deep genetic structure but no support for current taxonomic designation in a grasshopper species complex. Mol Ecol 28:3869–3886. https://doi.org/10.1111/mec.15189
Weston PH, Barker NP (2006) A new suprageneric classification of the Proteaceae, with an annotated checklist of genera. Telopea 11:314–344. https://doi.org/10.7751/telopea20065733
Acknowledgements
This research was funded by Main Roads Western Australia and Water Corporation. We thank Mike Hislop for discussions regarding C. caeruleum taxonomy.
Funding
This work was supported by Main Roads Western Australia and Water Corporation.
Author information
Authors and Affiliations
Contributions
A.W. and M.B. conceived the study. All authors collected samples. D.B. and R.M.B. analysed the data. D.B. wrote the manuscript. All authors contributed to interpretation of results and read the manuscript.
Corresponding author
Ethics declarations
Competing Interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Pradeep K. Divakar.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Bradbury, D., Binks, R.M., Webb, A. et al. Defining conservation units in a species complex with genomic-taxonomic discordance: a case study of Conospermum caeruleum (Proteaceae). Biodivers Conserv 32, 1949–1975 (2023). https://doi.org/10.1007/s10531-023-02585-z
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-023-02585-z