Significance

New species originate as populations become reproductively isolated from one another. Despite recent progress in uncovering the genetic basis of reproductive isolation, it remains unclear whether intrinsic reproductive barriers, such as hybrid sterility, can evolve as a by-product of local adaptation to contrasting environments. Here, we show that differences in a plant’s response to the pull of gravity have repeatedly evolved amongst coastal populations of an Australian wildflower, thus implicating a role of natural selection in their evolution. We found a strong genetic association between variation in this adaptive trait and hybrid sterility, suggesting that intrinsic reproductive barriers contribute to the origin of new species as populations adapt to heterogeneous environments.

Abstract

Natural selection is responsible for much of the diversity we see in nature. Just as it drives the evolution of new traits, it can also lead to new species. However, it is unclear whether natural selection conferring adaptation to local environments can drive speciation through the evolution of hybrid sterility between populations. Here, we show that adaptive divergence in shoot gravitropism, the ability of a plant’s shoot to bend upwards in response to the downward pull of gravity, contributes to the evolution of hybrid sterility in an Australian wildflower, Senecio lautus. We find that shoot gravitropism has evolved multiple times in association with plant height between adjacent populations inhabiting contrasting environments, suggesting that these traits have evolved by natural selection. We directly tested this prediction using a hybrid population subjected to eight rounds of recombination and three rounds of selection in the field. Our experiments revealed that shoot gravitropism responds to natural selection in the expected direction of the locally adapted population. Using the advanced hybrid population, we discovered that individuals with extreme differences in gravitropism had more sterile crosses than individuals with similar gravitropic responses, which were largely fertile, indicating that this adaptive trait is genetically correlated with hybrid sterility. Our results suggest that natural selection can drive the evolution of locally adaptive traits that also create hybrid sterility, thus revealing an evolutionary connection between local adaptation and the origin of new species.

Continue Reading

Data Availability

Sequence data have been deposited in The University of Queensland (https://espace.library.uq.edu.au/view/UQ:2c603c6).

Acknowledgments

We are grateful to S. Smith, L.H. Rieseberg, M. Cooper, J. Engelstaedter, M.A.F. Noor, C.L. Bywater and members of the D.O.-B. laboratory for insightful comments on previous versions of this manuscript. S. Karrenberg and S. Chenoweth provided instrumental feedback on M.J.W.’s PhD dissertation. We thank P. Brewer for his help in the design and execution of gravitropism experiments. We would also like to thank everyone that helped with the field selection experiments: E. Johnston, E. Monley, G. Wilkinson, P. Wilkinson, A. Mather, S. Thang, K. Giarola, G. Lebbink, E. Firkins-Barriere, P. Arnold, J. Donohoe, B. Brittain, H. Liu, D. Bernal, M.C. Melo, T. Richards, J. Walter, L. Ambrose, B. Ayalon, S. Carrol, M. Gallo, A. Maynard, C. Palmer, and S. Edgley.

Supporting Information

Appendix 01 (PDF)
Dataset_S01 (XLSX)
Dataset_S02 (XLSX)
Dataset_S03 (XLSX)
Dataset_S04 (XLSX)
Dataset_S05 (XLSX)
Dataset_S06 (XLSX)
Dataset_S07 (XLSX)
Dataset_S08 (XLSX)
Dataset_S09 (XLSX)

References

1
C. Darwin, On the Origins of Species by Means of Natural Selection (Murray, London, 1859).
2
J. A. Coyne, H. A. Orr, Speciation (Sinauer Associates, Sunderland, MA, 2004).
3
H. D. Rundle, M. C. Whitlock, A genetic interpretation of ecologically dependent isolation. Evolution 55, 198–201 (2001).
4
O. Seehausen et al., Genomics and the origin of species. Nat. Rev. Genet. 15, 176–192 (2014).
5
E. Baack, M. C. Melo, L. H. Rieseberg, D. Ortiz-Barrientos, The origins of reproductive isolation in plants. New Phytol. 207, 968–984 (2015).
6
J. M. Coughlan, D. R. Matute, The importance of intrinsic postzygotic barriers throughout the speciation process. Philos. Trans. R. Soc. Lond. B Biol. Sci. 375, 20190533 (2020).
7
D. Schluter, G. L. Conte, Genetics and ecological speciation. Proc. Natl. Acad. Sci. U.S.A. 106, 9955–9962 (2009).
8
D. B. Lowry, R. C. Rockwood, J. H. Willis, Ecological reproductive isolation of coast and inland races of Mimulus guttatus. Evolution 62, 2196–2214 (2008).
9
K. Bomblies, D. Weigel, Hybrid necrosis: Autoimmunity as a potential gene-flow barrier in plant species. Nat. Rev. Genet. 8, 382–393 (2007).
10
K. M. Wright, D. Lloyd, D. B. Lowry, M. R. Macnair, J. H. Willis, Indirect evolution of hybrid lethality due to linkage with selected locus in Mimulus guttatus. PLoS Biol. 11, e1001497 (2013).
11
M. Kirkpatrick, N. Barton, Chromosome inversions, local adaptation and speciation. Genetics 173, 419–434 (2006).
12
A. F. Agrawal, J. L. Feder, P. Nosil, Ecological divergence and the origins of intrinsic postmating isolation with gene flow. Int. J. Ecol. 2011, 435357 (2011).
13
A. Burt, R. Trivers, Genes in Conflict: The Biology of Selfish Genetic Elements (Harvard University Press, 2006).
14
S. A. Johnston, T. P. M. den Nijs, S. J. Peloquin, R. E. Hanneman Jr., The significance of genic balance to endosperm development in interspecific crosses. Theor. Appl. Genet. 57, 5–9 (1980).
15
D. C. Presgraves, The molecular evolutionary basis of species formation. Nat. Rev. Genet. 11, 175–180 (2010).
16
L. Fishman, A. L. Sweigart, When two rights make a wrong: The evolutionary genetics of plant hybrid incompatibilities. Annu. Rev. Plant Biol. 69, 707–731 (2018).
17
I. J. Radford, R. D. Cousens, P. W. Michael, Morphological and genetic variation in the Senecio pinnatifolius complex: Are variants worthy of taxonomic recognition? Aust. Syst. Bot. 17, 29–48 (2004).
18
I. Thompson, Taxonomic studies of Australian Senecio (Asteraceae): 5. The S. lautus/S. lautus complex. Muelleria 21, 23–76 (2005).
19
F. Roda et al., Convergence and divergence during the adaptation to similar environments by an Australian groundsel. Evolution 67, 2515–2529 (2013).
20
M. E. James et al., Phenotypic and genotypic parallel evolution in parapatric ecotypes of Senecio. Evolution. 10.1111/evo.14387 (2021).
21
M. Xu, L. Zhu, H. Shou, P. Wu, A PIN1 family gene, OsPIN1, involved in auxin-dependent adventitious root emergence and tillering in rice. Plant Cell Physiol. 46, 1674–1681 (2005).
22
J. G. Wallace et al., Genome-wide association for plant height and flowering time across 15 tropical maize populations under managed drought stress and well-watered conditions in Sub-Saharan Africa. Crop Sci. 56, 2365–2378 (2016).
23
A. Gallavotti, The role of auxin in shaping shoot architecture. J. Exp. Bot. 64, 2593–2608 (2013).
24
M. A. Domagalska, O. Leyser, Signal integration in the control of shoot branching. Nat. Rev. Mol. Cell Biol. 12, 211–221 (2011).
25
E. Sundberg, L. Østergaard, Distinct and dynamic auxin activities during reproductive development. Cold Spring Harb. Perspect. Biol. 1, a001628 (2009).
26
F. Roda, G. M. Walter, R. Nipper, D. Ortiz-Barrientos, Genomic clustering of adaptive loci during parallel evolution of an Australian wildflower. Mol. Ecol. 26, 3687–3699 (2017).
27
J. Friml, Auxin transport - Shaping the plant. Curr. Opin. Plant Biol. 6, 7–12 (2003).
28
D. Lopez, K. Tocquard, J.-S. Venisse, V. Legué, P. Roeckel-Drevet, Gravity sensing, a largely misunderstood trigger of plant orientated growth. Front Plant Sci 5, 610 (2014).
29
D. Sang et al., Strigolactones regulate rice tiller angle by attenuating shoot gravitropism through inhibiting auxin biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 111, 11199–11204 (2014).
30
G. M. Walter et al., Diversification across a heterogeneous landscape. Evolution 70, 1979–1992 (2016).
31
F. Roda et al., Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex. Mol. Ecol. 22, 2941–2952 (2013).
32
M. E. James et al., Highly replicated evolution of parapatric ecotypes. Mol. Biol. Evol. 38, 4805–4821 (2021).
33
M. C. Melo, A. Grealy, B. Brittain, G. M. Walter, D. Ortiz-Barrientos, Strong extrinsic reproductive isolation between parapatric populations of an Australian groundsel. New Phytol. 203, 323–334 (2014).
34
G. M. Walter et al., Loss of ecologically important genetic variation in late generation hybrids reveals links between adaptation and speciation. Evol. Lett. 4, 302–316 (2020).
35
M. Yamamoto, K. T. Yamamoto, Differential effects of 1-naphthaleneacetic acid, indole-3-acetic acid and 2,4-dichlorophenoxyacetic acid on the gravitropic response of roots in an auxin-resistant mutant of arabidopsis, aux1. Plant Cell Physiol. 39, 660–664 (1998).
36
I. Ottenschläger et al., Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc. Natl. Acad. Sci. U.S.A. 100, 2987–2991 (2003).
37
E. B. Blancaflor, Regulation of plant gravity sensing and signaling by the actin cytoskeleton. Am. J. Bot. 100, 143–152 (2013).
38
D. B. Lowry, D. Popovic, D. J. Brennan, L. M. Holeski, Mechanisms of a locally adaptive shift in allocation among growth, reproduction, and herbivore resistance in Mimulus guttatus. Evolution 73, 1168–1181 (2019).
39
L. Barboza et al., Arabidopsis semidwarfs evolved from independent mutations in GA20ox1, ortholog to green revolution dwarf alleles in rice and barley. Proc. Natl. Acad. Sci. U.S.A. 110, 15818–15823 (2013).
40
G. M. Walter et al., Senecio as a model system for integrating studies of genotype, phenotype and fitness. New Phytol. 226, 326–344 (2020).
41
M. Lynch, B. Walsh, Genetics and Analysis of Quantitative Traits (Sinaeur Associates Inc, Sunderland, MA, 1998).
42
P. Ranocha et al., Arabidopsis WAT1 is a vacuolar auxin transport facilitator required for auxin homoeostasis. Nat. Commun. 4, 2625 (2013).
43
P. Ranocha et al., Walls are thin 1 (WAT1), an Arabidopsis homolog of Medicago truncatula NODULIN21, is a tonoplast-localized protein required for secondary wall formation in fibers. Plant J. 63, 469–483 (2010).
44
X. Dai, K. Hayashi, H. Nozaki, Y. Cheng, Y. Zhao, Genetic and chemical analyses of the action mechanisms of sirtinol in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 102, 3129–3134 (2005).
45
M. Sagi, C. Scazzocchio, R. Fluhr, The absence of molybdenum cofactor sulfuration is the primary cause of the flacca phenotype in tomato plants. Plant J. 31, 305–317 (2002).
46
S. Promchuea, Y. Zhu, Z. Chen, J. Zhang, Z. Gong, ARF2 coordinates with PLETHORAs and PINs to orchestrate ABA-mediated root meristem activity in Arabidopsis. J. Integr. Plant Biol. 59, 30–43 (2017).
47
A. Sicard et al., Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella. Nat. Commun. 6, 7960 (2015).
48
A. L. Sweigart, L. E. Flagel, Evidence of natural selection acting on a polymorphic hybrid incompatibility locus in Mimulus. Genetics 199, 543–554 (2015).
49
W. Beeftink, J. Rozema, A. Huiskes, Ecology of Coastal Vegetation (Springer, 1985), vol. 6.
50
T. Auld, D. Morrison, Genetic determination of erect and prostrate growth habit in five shrubs from windswept headlands in the Sydney region. Aust. J. Bot. 40, 1–11 (1992).
51
D. Morrison, A. Rupp, Patterns of morphological variation within Acacia suaveolens (Mimosaceae). Aust. Syst. Bot. 8, 1013–1027 (1995).
52
G. M. Crutsinger, S. Y. Strauss, J. A. Rudgers, Genetic variation within a dominant shrub species determines plant species colonization in a coastal dune ecosystem. Ecology 91, 1237–1243 (2010).
53
T. Li et al., Calcium signals are necessary to establish auxin transporter polarity in a plant stem cell niche. Nat. Commun. 10, 726 (2019).
54
V. Naser, E. Shani, Auxin response under osmotic stress. Plant Mol. Biol. 91, 661–672 (2016).
55
T. van den Berg, R. A. Korver, C. Testerink, K. H. Ten Tusscher, Modeling halotropism: A key role for root tip architecture and reflux loop remodeling in redistributing auxin. Development 143, 3350–3362 (2016).
56
C. S. Galvan-Ampudia et al., Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23, 2044–2050 (2013).
57
B. A. Gould, Y. Chen, D. B. Lowry, Pooled ecotype sequencing reveals candidate genetic mechanisms for adaptive differentiation and reproductive isolation. Mol. Ecol. 26, 163–177 (2017).
58
D. B. Lowry, J. H. Willis, A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation. PLoS Biol. 8, e1000500 (2010).
59
D. B. Lowry, M. C. Hall, D. E. Salt, J. H. Willis, Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. 183, 776–788 (2009).
60
A. VanWallendael et al., A molecular view of plant local adaptation: Incorporating stress-response networks. Annu. Rev. Plant Biol. 70, 559–583 (2019).
61
M. Turelli, L. C. Moyle, Asymmetric postmating isolation: Darwin’s corollary to Haldane’s rule. Genetics 176, 1059–1088 (2007).
62
H.-H. Wang et al., Close arrangement of CARK3 and PMEIL affects ABA-mediated pollen sterility in Arabidopsis thaliana. Plant Cell Environ. 43, 2699–2711 (2020).
63
Y. Hou et al., Maternal ENODLs are required for pollen tube reception in Arabidopsis. Curr. Biol. 26, 2343–2350 (2016).
64
Y. Yang, U. Z. Hammes, C. G. Taylor, D. P. Schachtman, E. Nielsen, High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16, 1123–1127 (2006).
65
C. A. Schneider, W. S. Rasband, K. W. Eliceiri, NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671–675 (2012).
66
G. Rigó et al., Inactivation of plasma membrane-localized CDPK-RELATED KINASE5 decelerates PIN2 exocytosis and root gravitropic response in Arabidopsis. Plant Cell 25, 1592–1608 (2013).
67
A. M. Rashotte, S. R. Brady, R. C. Reed, S. J. Ante, G. K. Muday, Basipetal auxin transport is required for gravitropism in roots of Arabidopsis. Plant Physiol. 122, 481–490 (2000).
68
C. J. Geyer, S. Wagenius, R. G. Shaw, Aster models for life history analysis. Biometrika 94, 415–426 (2007).
69
R. G. Shaw, C. J. Geyer, S. Wagenius, H. H. Hangelbroek, J. R. Etterson, Unifying life-history analyses for inference of fitness and population growth. Am. Nat. 172, E35–E47 (2008).
70
R Core Team, R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2013).
71
J. D. Clarke, Cetyltrimethyl ammonium bromide (CTAB) DNA miniprep for plant DNA isolation. Cold Spring Harb. Protoc. 2009, pdb.prot5177 (2009).
72
H. Liu, “Developing genomic resources for an emerging ecological model species Senecio lautus,” PhD thesis, School of Biological Sciences, The University of Queensland (2015), 274 pp.
73
N. A. Baird et al., Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3, e3376 (2008).
74
B. Langmead, C. Trapnell, M. Pop, S. L. Salzberg, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 10, R25 (2009).
75
H. Li et al., The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078–2079 (2009).
76
S. F. Altschul, W. Gish, W. Miller, E. W. Myers, D. J. Lipman, Basic local alignment search tool. J. Mol. Biol. 215, 403–410 (1990).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 118 | No. 47
November 23, 2021
PubMed: 34789571

Classifications

Data Availability

Sequence data have been deposited in The University of Queensland (https://espace.library.uq.edu.au/view/UQ:2c603c6).

Submission history

Accepted: October 2, 2021
Published online: November 17, 2021
Published in issue: November 23, 2021

Keywords

  1. local adaptation
  2. intrinsic reproductive isolation
  3. hybrid sterility
  4. speciation
  5. natural selection

Acknowledgments

We are grateful to S. Smith, L.H. Rieseberg, M. Cooper, J. Engelstaedter, M.A.F. Noor, C.L. Bywater and members of the D.O.-B. laboratory for insightful comments on previous versions of this manuscript. S. Karrenberg and S. Chenoweth provided instrumental feedback on M.J.W.’s PhD dissertation. We thank P. Brewer for his help in the design and execution of gravitropism experiments. We would also like to thank everyone that helped with the field selection experiments: E. Johnston, E. Monley, G. Wilkinson, P. Wilkinson, A. Mather, S. Thang, K. Giarola, G. Lebbink, E. Firkins-Barriere, P. Arnold, J. Donohoe, B. Brittain, H. Liu, D. Bernal, M.C. Melo, T. Richards, J. Walter, L. Ambrose, B. Ayalon, S. Carrol, M. Gallo, A. Maynard, C. Palmer, and S. Edgley.

Notes

This article is a PNAS Direct Submission.

Authors

Affiliations

School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, QLD 4072, Australia;
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Departamento de Biología, Universidad Nacional de Colombia, Bogotá, Colombia;
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
School of Biological Sciences, Monash University, Melbourne VIC 3800, Australia;
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, QLD 4072, Australia;
Rick Nipper
Floragenex, Inc., Portland, OR 97239;
Floragenex, Inc., Portland, OR 97239;
Scott L. Allen
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Department of Zoology, University of Cambridge, Cambridge CB2 3EJ, United Kingdom
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, QLD 4072, Australia;
School of Biological Sciences, The University of Queensland, Brisbane QLD 4072, Australia;
Australian Research Council Centre of Excellence for Plant Success in Nature and Agriculture, The University of Queensland, Brisbane, QLD 4072, Australia;

Notes

2
To whom correspondence may be addressed. Email: [email protected].
Author contributions: M.J.W., F.R., G.M.W., C.A.B., and D.O.-B. designed research; M.J.W., F.R., G.M.W., M.E.J., R.N., J.W., S.L.A., H.L.N., and D.O.-B. performed research; M.J.W., F.R., G.M.W., M.E.J., and D.O.-B. contributed new reagents/analytic tools; M.J.W., F.R., G.M.W., and D.O.-B. analyzed data; and M.J.W., F.R., and D.O.-B. wrote the paper.
1
M.J.W. and F.R. contributed equally to this work.

Competing Interests

The authors declare no competing interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    Adaptive divergence in shoot gravitropism creates hybrid sterility in an Australian wildflower
    Proceedings of the National Academy of Sciences
    • Vol. 118
    • No. 47

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media