Abstract
Coevolution between interacting species is thought to increase biodiversity, but evidence linking microevolutionary processes to macroevolutionary patterns is scarce. We leveraged two decades of behavioral research coupled with historical DNA analysis to reveal that coevolution with hosts underpins speciation in brood-parasitic bronze-cuckoos. At a macroevolutionary scale, we show that highly virulent brood-parasitic taxa have higher speciation rates and are more likely to speciate in sympatry than less-virulent and nonparasitic relatives. We reveal the microevolutionary process underlying speciation: Hosts reject cuckoo nestlings, which selects for mimetic cuckoo nestling morphology. Where cuckoos exploit multiple hosts, selection for mimicry drives genetic and phenotypic divergence corresponding to host preference, even in sympatry. Our work elucidates perhaps the most common, but poorly characterized, evolutionary process driving biological diversification.
Original language | English |
---|---|
Pages (from-to) | 1030-1036 |
Number of pages | 7 |
Journal | Science |
Volume | 384 |
Issue number | 6699 |
DOIs | |
Publication status | Published - 30 May 2024 |
Externally published | Yes |
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In: Science, Vol. 384, No. 6699, 30.05.2024, p. 1030-1036.
Research output: Contribution to journal › Article › peer-review
TY - JOUR
T1 - Coevolution with hosts underpins speciation in brood-parasitic cuckoos
AU - Langmore, N. E.
AU - Grealy, A.
AU - Noh, H. J.
AU - Medina, I.
AU - Skeels, A.
AU - Grant, J.
AU - Murray, K. D.
AU - Kilner, R. M.
AU - Holleley, C. E.
N1 - Funding Information: We thank N. Knerr (Australian National Herbarium, CSIRO) for assistance photographing and digitizing collection eggshell specimens; N. Aitken (Centre for Ecogenomics and Bioinformatics, Australian National University) and T. McLay (Royal Botanic Gardens Victoria) for molecular advice; L. Joseph and I. Mason [Australian National Wildlife Collection (ANWC), CSIRO] for assistance with cuckoo identification; A. Grieve, A. Drew, C. Wilson, and J. Teh (ANWC) for curatorial assistance; J. Teh (ANWC), J. Davies, and Handbook of Australian New Zealand and Antarctic Birds, Oxford Univ. Press, for illustrations and G. Gullock for photography of adult specimens; E. Hahn (ANWC) for DNA extraction from adult tissue; Biomedical Resource Facility (ACT, Australia) for high-throughput DNA sequencing; L. Teasdale (Australian National Insect Collection, CSIRO) and A. Gofton for bioinformatic advice; J. Penalba, G. Olah, T. Suchan, and L. Neaves for analytical advice; V. Abernathy, F. Jacomb, G. Maurer, and B. Venables for assistance in the field; and L. Joseph for feedback on the manuscript. Funding: Australian Research Council DP180100021 (N.E.L., C.E.H., and R.M.K.); Holsworth Wildlife Research Endowment (H.-J.N.); National Geographic Society 9221- 12 (N.E.L.); and Centre for Biodiversity Analysis Ignition Grant, Australian National University (A.G., N.E.L., and C.E.H.). Author contributions: Conceptualization: N.E.L., C.E.H., and R.M.K.; Fieldwork: N.E.L., H.-J.N., and J.G.; Molecular genetic analyses: A.G., C.E.H., and K.D.M.; Macroevolutionary analyses: I.M. and A.S.; Funding acquisition: N.E.L., C.E.H., R.M.K., and A.G.; Project administration: N.E.L. and C.E.H.; Supervision: N.E.L. and C.E.H. Writing \u2013 original draft: N.E.L., C.E.H., A.G., and R.M.K.; Writing \u2013 review and editing: N.E.L., C.E.H., A.G., R.M.K., H.-J.N., J.G., K.D.M., I.M., and A.S. Competing interests: The authors declare that they have no competing interests. Data and materials availability: DNA sequences generated have been deposited within GenBank (available at ncbi.nlm.nih.gov) under the accession codes OQ363411-OQ363463. Sequencing reads have been deposited on NCBI\u2019s Sequence Read Archive (SRA) under the bioproject PRJNA926676 with the object identifier 32881702-32881744. Protocols are described in detail in the supplementary materials. Bioinformatic pipelines and scripts can be accessed from (57). All other data can be accessed through Dryad (58). Any registered specimens are freely accessible through loan requests through National Research Collections Australia, and all metadata for registered specimens is available through the Atlas of Living Australia (https://www.ala.org.au/). License information: Copyright \u00A9 2024 the authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original US government works. https://www.science. org/about/science-licenses-journal-article-reuse Publisher Copyright: © 2024 the authors, some rights reserved; exclusive licensee American Association for the Advancement of Science.
PY - 2024/5/30
Y1 - 2024/5/30
N2 - Coevolution between interacting species is thought to increase biodiversity, but evidence linking microevolutionary processes to macroevolutionary patterns is scarce. We leveraged two decades of behavioral research coupled with historical DNA analysis to reveal that coevolution with hosts underpins speciation in brood-parasitic bronze-cuckoos. At a macroevolutionary scale, we show that highly virulent brood-parasitic taxa have higher speciation rates and are more likely to speciate in sympatry than less-virulent and nonparasitic relatives. We reveal the microevolutionary process underlying speciation: Hosts reject cuckoo nestlings, which selects for mimetic cuckoo nestling morphology. Where cuckoos exploit multiple hosts, selection for mimicry drives genetic and phenotypic divergence corresponding to host preference, even in sympatry. Our work elucidates perhaps the most common, but poorly characterized, evolutionary process driving biological diversification.
AB - Coevolution between interacting species is thought to increase biodiversity, but evidence linking microevolutionary processes to macroevolutionary patterns is scarce. We leveraged two decades of behavioral research coupled with historical DNA analysis to reveal that coevolution with hosts underpins speciation in brood-parasitic bronze-cuckoos. At a macroevolutionary scale, we show that highly virulent brood-parasitic taxa have higher speciation rates and are more likely to speciate in sympatry than less-virulent and nonparasitic relatives. We reveal the microevolutionary process underlying speciation: Hosts reject cuckoo nestlings, which selects for mimetic cuckoo nestling morphology. Where cuckoos exploit multiple hosts, selection for mimicry drives genetic and phenotypic divergence corresponding to host preference, even in sympatry. Our work elucidates perhaps the most common, but poorly characterized, evolutionary process driving biological diversification.
UR - http://www.scopus.com/inward/record.url?scp=85194902111&partnerID=8YFLogxK
U2 - 10.1126/science.adj3210
DO - 10.1126/science.adj3210
M3 - Article
C2 - 38815013
AN - SCOPUS:85194902111
SN - 0036-8075
VL - 384
SP - 1030
EP - 1036
JO - Science
JF - Science
IS - 6699
ER -