Abstract
The current ecological crisis stemming from the loss of biodiversity and associated ecosystem services, highlights the urgency of documenting diversity and distribution. Bees are a classical example of an ecologically and economically important group, due to their high diversity and varied ecosystem services, especially pollination. Here, two common biodiversity indices, namely species richness and phylogenetic diversity, are evaluated geographically to determine the best approach for selecting areas of conservation priority. The model organisms used in this study are the North American species belonging to the bee genus Diadasia (Apidae). Based on the results obtained by analyzing distributional records and a molecular phylogeny, we can see that species richness and phylogenetic diversity are closely linked, although phylogenetic diversity provides a more detailed assessment of the spatial distribution of diversity. Therefore, while either one of these commonly used indices are valid as far as selecting areas of conservation priority, we recommend, if possible, to include genetic information in biodiversity and conservation studies.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on request.
References
Abascal F, Zardoya R, Telford MJ (2010) TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38:W7–13. https://doi.org/10.1093/nar/gkq291
Bailey RG (2004) Identifying ecoregion boundaries. Environ Manage 34:14–26. https://doi.org/10.1007/s00267-003-0163-6
Bailey RG (2014) Ecoregions: the Ecosystem Geography of the Oceans and Continents, Second edn. Springer, New York, N.Y.
Ballantyne G, Baldock KC, Willmer PG (2015) Constructing more informative plant–pollinator networks: visitation and pollen deposition networks in a heathland plant community. Proc R Soc B: Biol 282:20151130. https://doi.org/10.1098/rspb.2015.1130
Barreto E, Graham CH, Rangel TF (2019) Environmental factors explain the spatial mismatches between species richness and phylogenetic diversity of terrestrial mammals. Glob Ecol Biogeogr 28(12):1855–1865
Byrne P, Marek L (2020) Case Study: Sunflower Domestication and Breeding. Crop Wild Relatives in Genebanks. In: Volk G and Byrne P (Eds) Crop Wild Relatives and their Use in Plant Breeding. Colorado State University, Fort Collins, Colorado. Available at: https://colostate.pressbooks.pub/cropwildrelatives/chapter/case-study-sunflower-domestication-and-breeding/
Cadotte MW, Davies TJ (2010) Rarest of the rare: advances in combining evolutionary distinctiveness and scarcity to inform conservation at biogeographical scales. Divers Distrib 16:376–385. https://doi.org/10.1111/j.1472-4642.2010.00650.x
Cadotte MW, Dinnage R, Tilman D (2012) Phylogenetic diversity promotes ecosystem stability. Ecology 93:S223–S233. https://doi.org/10.1890/11-0426.1
Castresana J (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17:540–552. https://doi.org/10.1093/oxfordjournals.molbev.a026334
Commission for Environmental Cooperation (2009) Ecological Regions of Noth America. Available at: https://www.epa.gov/eco-research/ecoregions-north-america
Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (2017). Ecorregiones terrestres de M?xico 2008, modificado para el geoportal del SNIB. Comisi?n Nacional para el Conocimiento y Uso de la Biodiversidad. http://geoportal.conabio.gob.mx/metadatos/doc/html/ecorregionesmx.html
Connolly J, Cadotte MW, Brophy C, Dooley Á, Finn J, Kirwan L, Roscher C, Weigelt A (2011) Phylogenetically diverse grasslands are associated with pairwise interspecific processes that increase biomass. Ecology 92:1385–1392. https://doi.org/10.1890/10-2270.1
R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL https://www.R-project.org/
Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040. https://doi.org/10.1111/j.1461-0248.2010.01493.x
ESRI 2018. ArcGIS Desktop: release 10. Redlands, CA: Environmental Systems Research Institute
Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Conserv 61:1–10. https://doi.org/10.1016/0006-3207(92)91201-3
Flynn DFB, Mirotchnick N, Jain M, Palmer MI, Naeem S (2011) Functional and phylogenetic diversity as predictors of biodiversity- ecosystem-function relationships. Ecology 92:1573–1581. https://doi.org/10.1890/10-1245.1
Freitas FV, Branstetter MG, Casali DM, Aguiar AJC, Griswold T, Almeida EAB (2022) Phylogenomic dating and bayesian biogeography illuminate an antitropical pattern for eucerine bees. J Biogeogr 49(6):1034–1047. https://doi.org/10.1111/jbi.14359
Fritz SA, Rahbek C (2012) Global patterns of amphibian phylogenetic diversity. J Biogeogr 39(8):1373–1382
Gotelli NJ, Chao A (2013) Measuring and Estimating Species Richness, Species Diversity, and Biotic Similarity from Sampling Data. Encyclopedia of Biodiversity. Second Edition. Elsevier 195–212. https://doi.org/10.1016/B978-0-12-384719-5.00424-X
Grab H, Branstetter MG, Amon N, Urban-Mead KR, Park MG, Gibbs J, Blitzer EJ, Poveda K, Loeb G, Danforth BN (2019) Agriculturally dominated landscapes reduce bee phylogenetic diversity and pollination services. Science 363:282–284. https://doi.org/10.1126/science.aat6016
Hernandez-Rojas AC, Kluge J, Noben S, Reyes Chávez JD, Krömer T, Carvajal-Hernández CI, Salazar L, Kessler M (2021) Phylogenetic diversity of ferns reveals different patterns of niche conservatism and habitat filtering between epiphytic and terrestrial assemblages. Front Biogeogr 13(3):1–19. https://doi.org/10.21425/f5fbg50023
Honorio Coronado EN, Dexter KG, Pennington RT, Chave J, Lewis SL, Alexiades MN, Alvarez E, Alves de Oliveira A, Amaral IL, Araujo-Murakami A, Arets EJMM, Aymard GA, Baraloto C, Bonal D, Brienen R, Cerón C, Cornejo Valverde F, Di Fiore A, Farfan-Rios W, Feldpausch TR, Higuchi N, Huamantupa-Chuquimaco I, Laurance SG, Laurance WF, López-Gonzalez G, Marimon BS, Marimon-Junior BH, Monteagudo Mendoza A, Neill D, Palacios Cuenca W, Peñuela Mora MC, Pitman NCA, Prieto A, Quesada CA, Ramirez Angulo H, Rudas A, Ruschel AR, Salinas Revilla N, Salomão RP, Segalin, de Andrade A, Silman MR, Spironello W, ter Steege H, Terborgh J, Toledo M, Valenzuela Gamarra L, Vieira ICG, Vilanova Torre E, Vos V, Phillips OL (2015) Phylogenetic diversity of Amazonian tree communities. Diversity Distrib 21:1295–1307. https://doi.org/10.1111/ddi.12357
Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services (IPBES) (2016) The assessment report of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. Potts SG, Imperatriz-Fonseca VL, Ngo HT (Eds) Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. https://www.ipbes.net/assessment-reports/pollinators
Katoh K, Rozewicki J, Yamada KD (2019) MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization. Brief Bioinform 20:1160–1166. https://doi.org/10.1093/bib/bbx108
Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464. https://doi.org/10.1093/bioinformatics/btq166
Kumar S, Stecher G, Li M, Knyaz C, Tamura K (2018) MEGA X: Molecular Evolutionary Genetics Analysis across computing platforms. Mol Biol Evol 35:1547–1549. https://doi.org/10.1093/molbev/msy096
Laffan SW, Lubarsky E, Rosauer DF (2010) Biodiverse, a tool for the spatial analysis of biological and related diversity. Ecography 33:643–647. https://doi.org/10.1111/j.1600-0587.2010.06237.x
Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B (2017) PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol Biol Evol 34:772–773. https://doi.org/10.1093/molbev/msw260
Linsley EG, MacSwain JW (1957) The nesting habits, flower relationships, and parasites of some north american species of Diadasia (Hymenoptera: Anthophoridae). Wasmann J Biol 15:199–235. https://digitalcommons.usu.edu/bee_lab_all/19
Marek LF (2019) Crop wild relatives of sunflower in North America. In: Greene SL, Williams KA, Khoury CK, Kantar MB, Marek LF (eds) North american Crop Wild relatives. Important species, vol 2. Springer, New York, pp 453–483. https://link.springer.com/chapter/https://doi.org/10.1007/978-3-319-97121-6_14.
Matuoka MA, Benchimol M, Almeida-Rocha JM, Morante-Filho JC (2020) Effects of anthropogenic disturbances on bird functional diversity: a global meta-analysis. Ecol Indic 116:106471. https://doi.org/10.1016/j.ecolind.2020.106471
Michener CD (1979) Biogeography of the bees. Ann Mo Bot Gar 66:277–347. https://doi.org/10.2307/2398833
Miklós I, Podani J (2004) Randomization of presence–absence matrices: comments and new algorithms. Ecology 85:86–92. https://doi.org/10.1890/03-0101
Minckley RL (2008) Faunal composition and species richness differences of bees (Hymenoptera: Apiformes) from two north american regions. Apidologie 39:176–188. https://doi.org/10.1051/apido:2007062
Minckley RL, Radke WR (2021) Extreme species density of bees (Apiformes, Hymenoptera) in the warm deserts of North America. J Hymenopt Res 82:317–345. https://doi.org/10.3897/jhr.82.60895
Mouillot D, Graham NA, Villéger S, Mason NW, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177. https://doi.org/10.1016/j.tree.2012.10.004
Murphy GEP, Romanuk TN (2014) A meta-analysis of declines in local species richness from human disturbances. Ecol Evol 4:91–103. https://doi.org/10.1002/ece3.909
Naeem S, Duffy JE, Zavaleta E (2012) The functions of biological diversity in an age of extinction. Science 336:1401–1406. https://doi.org/10.1126/science.1215855
Nobel A, Lizin S, Brouwer R, Bruns SB, Stern DI, Malina R (2020) Are biodiversity losses valued differently when they are caused by human activities? A meta-analysis of the non-use valuation literature. Environ Res Lett 15:073003. https://doi.org/10.1088/1748-9326/ab8ec2
Obrist MK, Duelli P (2010) Rapid biodiversity assessment of arthropods for monitoring average local species richness and related ecosystem services. Biodiv Cons 19:2201–2220. https://doi.org/10.1007/s10531-010-9832-y
Paradis E, Schliep K (2019) Ape 5.0: an environment for modern phylogenetics and evolutionary analyses. R Bioinf 35:526–528. https://doi.org/10.1093/bioinformatics/bty633
Parys K, Griswold T, Ikerd H, Orr M (2018) New records and range extensions of several species of native bees (Hymenoptera: Apoidea) from Mississippi. Biodivers Data J 6:e25230. https://doi.org/10.3897/bdj.6.e25230
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904. https://doi.org/10.1093/sysbio/syy032
Rodrigues A, Brooks T, Gaston K (2005) Integrating phylogenetic diversity in the selection of priority areas for conservation: does it make a difference? In: Purvis A, Gittleman J, Brooks T (eds) Phylogeny and conservation. Conservation Biology. Cambridge University Press, Cambridge, pp 101–119. doi:https://doi.org/10.1017/CBO9780511614927.005
RStudio Team (2021) RStudio: Integrated Development for R. RStudio, PBC, Boston, MA. http://www.rstudio.com/
Safi K, Cianciaruso MV, Loyola RD, Brito D, Armour-Marshall K, Diniz-Filho JAF (2011) Understanding global patterns of mammalian functional and phylogenetic diversity. Philos T R Soc B 366:2536–2544. https://doi.org/10.1098/rstb.2011.0024
Sipes SD, Tepedino VJ (2005) Pollen-host specificity and evolutionary patterns of host switching in a clade of specialist bees (Apoidea: Diadasia). Biol J Linn Soc 86:487–505. https://doi.org/10.1111/j.1095-8312.2005.00544.x
Sipes SD, Wolf PG (2001) Phylogenetic relationships within Diadasia, a group of specialist bees. Mol Phylogenet Evol 19:144–156. https://doi.org/10.1006/mpev.2001.0914
Smiley TM, Title PO, Zelditch ML, Terry RC (2020) Multi-dimensional biodiversity hotspots and the future of taxonomic, ecological and phylogenetic diversity: a case study of north american rodents. Glob Ecol Biogeogr 29(3):516–533
Su YS, Yajima M, Su MYS (2015) Package ‘R2jags’. R package version 0.03-08, Available at: http://CRAN. R-project. org/package = R2jags
Suchard MA, Lemey P, Baele G, Ayres DL, Drummond AJ, Rambaut A (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10 Virus Evol 4:vey016. https://doi.org/10.1093/ve/vey016
Tucker CM, Cadotte MW (2013) Unifying measures of biodiversity: understanding when richness and phylogenetic diversity should be congruent. Divers Distr 19:845–854. https://doi.org/10.1111/ddi.12087
US Department of Agriculture (2015) Natural Resource Conservation Service, US Geological Survey & Environmental Protection Agency - Watershed Boundary Dataset. Colorado State University.
Vane-Wright RI, Humphries CJ, Williams PH (1991) What to protect?—Systematics and the agony of choice. Biol Cons 553:235–254. https://doi.org/10.1016/0006-3207(91)90030-D
Venail P, Gross K, Oakley TH, Narwani A, Allan E, Flombaum P, Isbell F, Joshi J, Reich PB, Tilman D, Van Ruijven J (2015) Species richness, but not phylogenetic diversity, influences community biomass production and temporal stability in a re-examination of 16 grassland biodiversity studies. Funct Ecol 29:615–626. https://doi.org/10.1111/1365-2435.12432
Wiken E, Jiménez Nava F, Griffith G (2011) North American Terrestrial Ecoregions—Level III. Commission for Environmental Cooperation, Montreal, Canada. http://www.cec.org/north-american-environmental-atlas/terrestrial-ecoregions-level-iii/
Wilson JS, Carril OM, Sipes SD (2014) Revisiting the great american biotic interchange through analyses of amphitropical bees. Ecography 37:791–796. https://doi.org/10.1111/ecog.00663
Winter M, Devictor V, Schweiger O (2013) Phylogenetic diversity and nature conservation: where are we? Trends Ecol Evol 28:4:199–204. https://doi.org/10.1016/j.tree.2012.10.015
Wong JS, Chan YS, Ng CL, Tun KP, Darling ES, Huang D (2018) Comparing patterns of taxonomic, functional and phylogenetic diversity in reef coral communities. Coral Reefs 37:737–750
Xu MZ, Yang LH, Kong HH, Wen F, Kang M (2019a) Congruent spatial patterns of species richness and phylogenetic diversity in karst flora: Case study of Primulina (Gesneriaceae). J Syst Evol 59(2):251–261
Xu Y, Huang J, Lu X, Ding Y, Zang R (2019b) Priorities and conservation gaps across three biodiversity dimensions of rare and endangered plant species in China. Biol Cons 229:30–37
Acknowledgements
The authors acknowledge William H. Clark and Luz Abril Garduño for English language editing and the editor and two anonymous reviewers for their valuable observations and comments on the manuscript. We are also grateful to Eulogio López, Edna Arvizu, Heriberto Murillo, for their help in the sampling effort. We also thank JiJi Foundation for the grant 20200201 to the project “Diversity of Bees of Baja California” and the Consejo Nacional de Ciencia y Tecnología for the grant CB2017-2018_A1-S-15134 to FSC and for the master’s scholarship 747190 to Diego de Pedro. Our own samplings were made under the Secretaría de Medio Ambiente y Recursos Naturales collecting license SGPA/DGVS/11596/17.
Funding
This work was supported by the JiJi Foundation (grant number 20200201, project “Diversity of Bees of Baja California”) and the Consejo Nacional de Ciencia y Tecnología (grant number CB2017-2018_A1-S-15134 to FSC and master’s scholarship 747190 to DEdP).
Author information
Authors and Affiliations
Contributions
Diego de Pedro and Fadia Sara Ceccarelli contributed to the study conception and design. Data collection and analysis were performed by Diego de Pedro, Fadia Sara Ceccarelli, Rémy Vandame, Jorge Mérida and Philippe Sagot. The first draft of the manuscript was written by Diego de Pedro and Fadia Sara Ceccarelli and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Akihiro Nakamura.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
de Pedro, D., Ceccarelli, F.S., Vandame, R. et al. Congruence between species richness and phylogenetic diversity in North America for the bee genus Diadasia (Hymenoptera: Apidae). Biodivers Conserv 32, 4445–4459 (2023). https://doi.org/10.1007/s10531-023-02706-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-023-02706-8