Architectural constraints, male fertility variation and biased floral morph ratios in tristylous populations

Abstract

Tristyly is a genetic polymorphism in which populations are comprised of three floral morphs (mating types) differing reciprocally in sex-organ height. Intermorph (disassortative) mating governed by a trimorphic incompatibility system should result in 1:1:1 morph ratios at equilibrium, but both deterministic and stochastic processes can cause skewed morph ratios in tristylous populations. Here, we investigate mechanisms causing morph-ratio bias in Pontederia parviflora, an emergent aquatic native to tropical America. We compared reproductive traits among morphs and surveyed 71 populations to determine patterns of morph-ratio bias. We then used simulation models of morph-frequency dynamics to test the hypothesis that morph-specific differences in pollen production and their influence on male fertility can explain patterns of morph-ratio bias. Ninety-seven percent of populations that we sampled were tristylous, but with a significant excess of the short-styled morph and a deficiency of the long-styled morph. Atypically for a tristylous species, mid-level anthers of the short-styled morph produced over twice as much pollen compared with the corresponding anthers of the long-styled morph. Our computer models incorporating this difference in male fertility resulted in morph ratios not significantly different from the average frequencies from our survey suggesting that the short-styled morph is more successful than the long-styled morph in siring ovules of the mid-styled morph. We propose that the difference in male fertility between morphs may be a non-adaptive consequence of a developmental constraint caused by the architecture of tristyly in Pontederiaceae.

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Acknowledgements

This research was supported by Special Visiting Researcher grant (88881.062191/2014-01) from Science Without Borders Program (CAPES and CNPq) and a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to S.C.H.B. A Special Visiting Researcher grant enabled S.C.H.B. to conduct fieldwork in the Pantanal and support a post-doctoral grant to N.L.C. (88887.067088/2014-00). We thank Milena Delatorre for assistance with field sampling, Martin Morgan for providing software used in our computer simulations, Erich Fischer for encouragement.

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NLC and SCHB planned the research and conducted the fieldwork, NLC analyzed the data and NLC and SCHB wrote the manuscript.

Correspondence to Nicolay Leme da Cunha.

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da Cunha, N.L., Barrett, S.C.H. Architectural constraints, male fertility variation and biased floral morph ratios in tristylous populations. Heredity 123, 694–706 (2019). https://doi.org/10.1038/s41437-019-0237-8

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