Evolution of dioecy: can nuclear–cytoplasmic interactions select for maleness?

Maurice, Sandrine; Belhassen, E.; Couvet, Denis; Gouyon, Pierre‐Henri

doi:10.1038/hdy.1994.181

Cited by 74 publications

(60 citation statements)

References 24 publications

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“…This reproductive system has evolved many times independently in flowering plants (reviewed by Renner and Ricklefs (1995)). Gynodioecy may sometimes be a step in the evolutionary route from hermaphroditism to dioecy (reviewed by Barrett (2002)) and several theoretical studies have shown that nucleo-cytoplasmic gynodioecy (as in S. nutans) can evolve towards dioecy, through the replacement of hermaphrodites by males (Maurice et al, 1994;Schultz, 1994). Although this evolutionary transition has received little empirical support (Spigler and Ashman, 2012), it could have occurred in the genus Silene.…”

Section: Discussionmentioning

confidence: 99%

Disentangling the effects of mating systems and mutation rates on cytoplamic diversity in gynodioecious Silene nutans and dioecious Silene otites

et al. 2013

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Many flowering plant species exhibit a variety of distinct sexual morphs, the two most common cases being the co-occurrence of females and males (dioecy) or the co-occurrence of hermaphrodites and females (gynodioecy). In this study, we compared DNA sequence variability of the three genomes (nuclear, mitochondrial and chloroplastic) of a gynodioecious species, Silene nutans, with that of a closely related dioecious species, Silene otites. In the light of theoretical models, we expect cytoplasmic diversity to differ between the two species due to the selective dynamics that acts on cytoplasmic genomes in gynodioecious species: under an epidemic scenario, the gynodioecious species is expected to exhibit lower cytoplasmic diversity than the dioecious species, while the opposite is expected in the case of balancing selection maintaining sterility cytoplasms in the gynodioecious species. We found no difference between the species for nuclear gene diversity, but, for the cytoplasmic loci, the gynodioecious S. nutans had more haplotypes, and higher nucleotide diversity, than the dioecious relative, S. otites, even though the latter has a relatively high rate of mitochondrial synonymous substitutions, and therefore presumably a higher mutation rate. Therefore, as the mitochondrial mutation rate cannot account for the higher cytoplasmic diversity found in S. nutans, our findings support the hypothesis that gynodioecy in S. nutans has been maintained by balancing selection rather than by epidemic-like dynamics.

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Section: Discussionmentioning

confidence: 99%

Disentangling the effects of mating systems and mutation rates on cytoplamic diversity in gynodioecious Silene nutans and dioecious Silene otites

et al. 2013

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“…Because the thrum haplotype is dominant over the pin one (Ganders 1979b), restorer genes would not be expressed in thrum plants, producing thrum-biased male sterility. Restorer alleles would only be expressed in pin individuals, and therefore, the costs of restoration (the deleterious pleiotropic effects of the nuclear restorers, Charlesworth 1991;Maurice et al 1994) would only be paid by plants expressing this morph.…”

Section: Discussionmentioning

confidence: 99%

“…Male sterility in gynodioecious species is often determined by the interaction of nuclear and cytoplasmic genes (Saumitou-Laprade et al 1994;Schultz 1994;Manicacci et al 1996; Thompson et al 1998). Theoretical models have shown that dioecy evolves in less restrictive conditions when it originates from nuclear-cytoplasmic gynodioecy than from other forms of genetic determination (Maurice 1992;Maurice et al 1994;Schultz 1994). In fact, gynodioecy could be a common pathway in the evolution of gender specialization in plants because it represents one of the three mutations required for dioecy to evolve (Schultz 1994).…”

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confidence: 99%

“…Sex-linked genetic effects can also affect gender specialization and greatly influence the outcome of selection on sexual phenotypes (Cosmides and Tooby 1989;Frank 1989;Maurice et al 1994;Schultz 1994). Gynodioecy, a reproductive polymorphism characterized by the simultaneous presence of hermaphrodite and female (male-sterile) individ-uals, has frequently been proposed as an intermediate evolutionary step between hermaphroditism and dioecy (Lloyd 1975;Charlesworth, and Charlesworth 1978;Schultz 1994;Webb 1999).…”

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confidence: 99%

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Parental Effects and Gender Specialization in a Tropical Heterostylous Shrub

Ávila-Sakar

Domínguez²

2000

Evolution

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Abstract. Male sterility in hermaphroditic species may represent the first step in the evolution toward dioecy. However, gender specialization will not proceed unless the male-sterile individuals compensate for fitness lost through the male function with an increase in fitness through the female function. In the distylous shrub Erythroxylum havanense, thrum plants are partially male-sterile. Using data collected throughout eight years, we investigated whether thrum individuals have an increased performance as female parents, thereby compensating for their loss of male fitness. We found that thrum plants outperformed pins in the probabilities of seed maturation and germination and long-term growth of the seedlings. In turn, pollen from pin plants achieved greater pollen tube growth rates. Our results suggest that the superior performance of the progeny of thrum maternal plants is a consequence of better seed provisioning via effects of the maternal environment, cytotype or nuclear genes. Overall, our results suggest that E. havanense is evolving toward a dioecious state through a gynodioecious intermediate stage. This evolutionary pathway is characterized by an unusual pattern of gender dimorphism with thrums becoming females and pins becoming males. We propose that this pattern may be better explained by the interaction between male-sterility cytoplasmic genes and the heterostyly supergene.

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“…In populations that are polymorphic at both the CMS and nuclear restorer loci, sex is determined by the epistatic interaction between these loci [25,26]. Sex determination can become nuclear if selection sweeps the male sterile cytoplasm to fixation, leaving the nuclear restorer gene polymorphic [27,28]. Thus, fixation of the CMS cytotype and evolution of nuclear sex-determination can also be viewed as a critical prerequisite for the evolution of dioecy.…”

Section: Introductionmentioning

confidence: 99%

The effect of disease on the evolution of females and the genetic basis of sex in populations with cytoplasmic male sterility

Miller

Bruns

2016

Proc. R. Soc. B.

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The evolution of separate males and females is an important evolutionary transition that has occurred multiple times in flowering plants. While empirical studies have stressed the potential importance of natural enemies and organismal interactions in the evolution of separate sexes, there has been no treatment of natural enemies in the theoretical literature. We investigated the effects of disease on the evolution of females in gynodioecious populations composed of females and hermaphrodites, where sex is determined by the interaction of cytoplasmic male sterility (CMS) and nuclear restorer genes. When females are significantly more resistant than hermaphrodites, disease drives an increase in the frequency of females and sex determination becomes nuclear, creating the pre-conditions for the evolution of separate males and females. However, when females are only moderately more resistant, disease drives changes in the frequency of CMS and restorer alleles, but has little effect on the frequency of females. We discuss our results in the context of the evolution of mating systems and cyto-nuclear epistasis.

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Evolution of dioecy: can nuclear–cytoplasmic interactions select for maleness?

Cited by 74 publications

References 24 publications

Disentangling the effects of mating systems and mutation rates on cytoplamic diversity in gynodioecious Silene nutans and dioecious Silene otites

Disentangling the effects of mating systems and mutation rates on cytoplamic diversity in gynodioecious Silene nutans and dioecious Silene otites

Parental Effects and Gender Specialization in a Tropical Heterostylous Shrub

The effect of disease on the evolution of females and the genetic basis of sex in populations with cytoplasmic male sterility

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