Direct and indirect selection on mate choice during pollen competition: Effects of male and female sexual traits on offspring performance following two‐donor crosses

Madjidian, Josefin A.; Smith, Henrik G.; Andersson, Stefan; Lankinen, Åsa

doi:10.1111/jeb.13684

Cited by 7 publications

(6 citation statements)

References 80 publications

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“…Moreover, there is an abundance of existing ecological and phenotypic data on Collinsia species related to niche breadth ( Randle et al 2009 ; Grant and Kalisz 2020 ), sexual interference, sexual conflict, and pollen traits ( e.g. , Lankinen and Madjidian 2011 ; Lankinen et al 2016 ; Lankinen and Strandh 2019 ; Malagon et al 2019 ; Madjidian et al 2020 ), pollination biology ( e.g. , Elle and Carney 2003 ; Kalisz and Vogler 2003 ; Kalisz et al 2004 ; Randle et al 2018 ), phenotypic plasticity ( Jorgensen and Arathi 2013 ; Spigler and Kalisz 2013 ), population differentiation ( Hazzouri et al .…”

Section: Discussionmentioning

confidence: 99%

New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species

Frazee

Rifkin

Maheepala

et al. 2021

G3 Genes|Genomes|Genetics

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The evolutionary transition from outcross-fertilization to self-fertilization is one of the most common in angiosperms and is often associated with a parallel shift in floral morphological and developmental traits, such as reduced flower size and pollen to ovule ratios, known as the ‘selfing syndrome’. How these convergent phenotypes arise, the extent to which they are shaped by selection, and the nature of their underlying genetic basis are unsettled questions in evolutionary biology. The genus Collinsia (Plantaginaceae) includes seven independent transitions from outcrossing or mixed mating to high selfing rates accompanied by selfing syndrome traits. Accordingly, Collinsia represents an ideal system for investigating this parallelism, but requires genomic resource development. We present a high quality de novo genome assembly for the highly selfing species C. rattanii. To begin addressing the basis of selfing syndrome developmental shifts, we evaluate and contrast patterns of gene expression from floral transcriptomes across three stages of bud development for C. rattanii and its outcrossing sister species C. linearis. Relative to C. linearis, total gene expression is less variable among individuals and bud stages in C. rattanii. In addition, there is a common pattern among differentially expressed genes: lower expression levels that are more constant across bud development in C. rattanii relative to C. linearis. Transcriptional regulation of enzymes involved in pollen formation specifically in early bud development may influence floral traits that distinguish selfing and outcrossing Collinsia species through pleiotropic functions. Future work will include additional Collinsia outcrossing-selfing species pairs to identify genomic signatures of parallel evolution.

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Section: Discussionmentioning

confidence: 99%

New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species

Frazee

Rifkin

Maheepala

et al. 2021

G3 Genes|Genomes|Genetics

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“…This conclusion was reached in an influential theoretical paper by Kirkpatrick and Barton (1997), and was later arrived at by a somewhat different line of reasoning by Cameron et al (2003). It has since become widely accepted (e.g., Kokko et al 2006;Hettyey et al 2010;Kuijper et al 2012;Ryan and Cummings 2013;Kiyose et al 2015;Rosenthal 2017;Fitzpatrick and Servedio 2018;Suzaki et al 2018;Svensson 2019;Kelly and Adam-Granger 2020;Madjidian et al 2020). For example, in a review of sexual selection theory, Kuijper et al (2012) cite both Kirkpatrick and Barton (1997) and Cameron et al (2003) in support of the statement that "even slight costs can override indirect benefits of choosiness, leading to the theoretical expectation that sexual selection driven only by indirect benefits of choosiness is rare in nature."…”

Section: Impact Summarymentioning

confidence: 98%

“… 2018 ; Svensson 2019 ; Kelly and Adam‐Granger 2020 ; Madjidian et al. 2020 ). For example, in a review of sexual selection theory, Kuijper et al.…”

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confidence: 99%

A reexamination of theoretical arguments that indirect selection on mate preference is likely to be weaker than direct selection

Fry

2022

Evolution Letters

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Female preference for male ornaments or displays can evolve by indirect selection resulting from genetic benefits of mate choices, or by direct selection resulting from nongenetic benefits or selection on sensory systems occurring in other contexts. In an influential paper, Kirkpatrick and Barton used a good‐genes model and evolutionary rates estimated from the fossil record to conclude that indirect selection on preference is likely to be weak compared to typical strengths of direct selection. More recent authors have extrapolated from Kirkpatrick and Barton's conclusions to suggest that the presence of preference‐trait genetic correlations in equations for indirect but not direct selection gives a purely theoretical basis to the conclusion that the former is likely to be weaker than the latter. Here, I challenge these views, and argue that the relative importance of direct and indirect selection on preference is an empirical issue that defies simple generalizations. First, I show that Kirkpatrick and Barton based their conclusion on a questionable claim about typical rates of evolution due to direct selection. Second, I argue that claiming that direct selection on preference is stronger than indirect selection because only equations for the latter contain a genetic correlation mistakes the mathematical simplicity with which direct selection is usually represented for evidence regarding its magnitude. By comparing a simple equation for the selection response of preference caused by somatic (“direct”) benefits to Kirkpatrick and Barton's result for the response to indirect selection, I show that indirect selection on preference is not inherently weaker than direct selection. I also point out an important but overlooked reason why selection on preference under the sensory bias hypothesis can be expected to be less effective in the long run than that from either somatic or genetic benefits of mate choices.

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“…Therefore, in principle, sexual selection could operate after pollination through both male–male competition and female choice. Males with higher pollen performance traits may be at an advantage against other males (Mazer et al ., 2010; Baskin & Baskin, 2015), while females, via pistil traits and chemical signalling, could exhibit choosiness among different pollen (Lankinen & Strandh, 2016; Mazer et al ., 2016; Madjidian et al ., 2020). We will further explore below whether such mechanisms can establish postmating reproductive barriers, and potentially lead to speciation.…”

Section: Sexual Selection Mechanisms and Reproductive Strategies In P...mentioning

confidence: 99%

“…Runaway selection may lead to faster divergence of pollen–pistil communication mechanisms that result in the emergence of pollen–pistil incompatibilities (Arnold et al ., 1993; Carney, Hodges & Arnold, 1996; Klips, 1999) and speciation. Finally, sexually driven divergence in pollen performance and female choosiness (Diaz & Macnair, 1999; Runions & Geber, 2000; Mazer et al ., 2018; Madjidian et al ., 2020) may produce unilateral pollen–pistil incompatibilities (Covey et al ., 2010; Baek et al ., 2015) which result in speciation. For example, the change in pollination mode from biotic to abiotic is correlated with a decreasing speciation rate (Dodd et al ., 1999).…”

Section: Sexual Selection and Plant Speciation (Macroevolutionary Scale)mentioning

confidence: 99%

Darwin's ‘mystery of mysteries’: the role of sexual selection in plant speciation

Haghighatnia,

Machac,

Schmickl

et al. 2023

Biological Reviews

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Sexual selection is considered one of the key processes that contribute to the emergence of new species. While the connection between sexual selection and speciation has been supported by comparative studies, the mechanisms that mediate this connection remain unresolved, especially in plants. Similarly, it is not clear how speciation processes within plant populations translate into large‐scale speciation dynamics. Here, we review the mechanisms through which sexual selection, pollination, and mate choice unfold and interact, and how they may ultimately produce reproductive isolation in plants. We also overview reproductive strategies that might influence sexual selection in plants and illustrate how functional traits might connect speciation at the population level (population differentiation, evolution of reproductive barriers; i.e. microevolution) with evolution above the species level (macroevolution). We also identify outstanding questions in the field, and suitable data and tools for their resolution. Altogether, this effort motivates further research focused on plants, which might potentially broaden our general understanding of speciation by sexual selection, a major concept in evolutionary biology.

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Direct and indirect selection on mate choice during pollen competition: Effects of male and female sexual traits on offspring performance following two‐donor crosses

Cited by 7 publications

References 80 publications

New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species

New genomic resources and comparative analyses reveal differences in floral gene expression in selfing and outcrossing Collinsia sister species

A reexamination of theoretical arguments that indirect selection on mate preference is likely to be weaker than direct selection

Darwin's ‘mystery of mysteries’: the role of sexual selection in plant speciation

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