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Evidence from the Dioecious Cape Genus Leucadendron (Proteaceae)

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Evidence from the Dioecious Cape Genus Leucadendron (Proteaceae) bioRxiv preprint doi: https://doi.org/10.1101/212555; this version posted November 1, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 1 1 Equality between the sexes in plants for costs of reproduction; evidence from the dioecious 2 Cape genus Leucadendron (Proteaceae). 3 Jeremy J. Midgley*1, Adam G. West1, Michael D. Cramer1 4 1Dept Biological Sciences, University of Cape Town, P bag Rondebosch 7701, South Africa 5 [email protected]; [email protected]; [email protected]. 6 Keywords Life history evolution, plants, sexual allocation, dioecy, Leucadendron, 7 dimorphism 8 Running title: Equality between the sexes in plants 9 bioRxiv preprint doi: https://doi.org/10.1101/212555; this version posted November 1, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 2 10 Abstract 11 It has been argued that sexual allocation is greater for female function than male function in 12 plants in general and specifically for the large dioecious Cape genus Leucadendron. Here, 13 we use new interpretations of published information to support the hypothesis of equality 14 between sexes in this genus. The explanations are based on the fire ecology of the Cape that 15 results in reproductive synchrony, reproductive doubling and competitive symmetry. Firstly, 16 strict post-fire seedling establishment of the reseeder life-history in the Cape results in single- 17 aged populations. Consequently, the reproductive and vegetative schedules of males must 18 synchronously track that of females. This implies equal allocation to sex. Secondly, after 19 fires, dioecious females have double the seedling to adult ratio of co-occurring 20 hermaphrodites. This indicates that being liberated from male function allows females access 21 to resources that double their fitness compared to hermaphrodites. Therefore, male and 22 female costs of reproduction are equal in hermaphrodites. Thirdly, competitive symmetry 23 must occur because males and female plants will frequently encounter each other as close 24 near neighbours. Competitive asymmetry would both reduce mating opportunities and skew 25 local sex ratios. The evidence to date is for 1:1 sex ratios in small plots and this indicates 26 competitive symmetry and a lack of dimorphic niches. Finally, vegetatively dimorphic 27 species must also allocate equally to sex, or else sexual asynchrony, lack of reproductive 28 doubling or competitive asymmetry will occur. 29 30 bioRxiv preprint doi: https://doi.org/10.1101/212555; this version posted November 1, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 3 31 Introduction 32 Understanding allocation by the different sexes is a key focus in evolutionary studies and in 33 organisms where both parents contribute genes equally to off-spring, sexual allocation (e.g. 34 sex ratios, parental care of off-spring of different sexes, costs of reproduction) is expected to 35 be equal (Fischerian) (Hamilton 1967; Charnov 1982). It is difficult to investigate sexual 36 allocation in plants because most plants (>90%) are hermaphrodites, nevertheless, it is 37 generally assumed that the resource costs of reproduction are greater for females (Barrett and 38 Hough 2013). Although only female plants bear the costs of producing large seeds, fruits and 39 cones after flowering, it is nevertheless controversial whether total female costs are higher 40 than male costs. For example, Harris and Pannell (2010) argued that serotiny (storage of 41 seeds in closed cones that open after plant death in fire) is a form of maternal care that 42 imposes extra selection pressure on females of the Cape Proteaceae genus Leucadendron for 43 greater water efficiency. They also argue that vegetative dimorphism, such as the larger 44 leaves and lower rates of branching in females, results from this extra ecophysiological 45 selection on females. Cones on females need to maintain a water supply to prevent them from 46 drying out during the dry, hot Mediterranean summers and opening prematurely and thus 47 releasing seeds into the unfavourable inter-fire environment. The proposed mechanism for 48 greater water efficiency in females is the hydraulic benefit of their less frequent branching 49 than occurs in males. Barrett et al. (2010) noted that males in serotinous L. gandogeri 50 matured first and argued that the delayed maturation of females reflects their higher costs of 51 reproduction. 52 In contrast to these suggestions of higher female costs, Midgley (2010) showed that δ 13 C (an 53 integrated measure of an individual’s water use efficiency) did not differ between males and 54 females of eight Leucadendron species, including a co-occurring vegetatively monomorphic 55 and very dimorphic species, as well as serotinous and non-serotinous species. Midgley (2010) 56 also argued that vegetative dimorphism in leaf size and branching is not explained by 57 ecophysiological differences between the sexes, but differences in the process of pollen 58 transfer and capture. Thus, whether the costs of sex are higher for females and whether this 59 could lead to vegetative dimorphism is unresolved for Leucadendron. Here we use new 60 interpretations of published data to further support the hypothesis that the costs of sex are 61 equal amongst the sexes. Our hypothesis for sexual equality should apply generally to all 62 plants and could be tested using some of the many hundreds of Cape dioecious species (such bioRxiv preprint doi: https://doi.org/10.1101/212555; this version posted November 1, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 4 63 as > 300 Restionaceae species) and using dioecious species from other similarly fire-prone 64 environments such as in Western Australia. 65 The hypothesis of higher allocation to reproduction in female plants, besides being of 66 fundamental evolutionary interest, may also have a conservation implication for dioecious 67 taxa such as Leucadendron. It has been argued that global change will lead to a decline in 68 dioecious species (Hultine et al. 2016). A more stressed future environment (e.g. greater 69 aridity) is argued to favour male survival if males allocate relatively more to vegetative 70 growth and less to reproduction than females. Female biased mortality will then have 71 negative population consequences such as male biased sex ratios. 72 The fire-prone vegetation of the Cape (fynbos), South Africa, is an excellent place to 73 test the hypothesis of greater female allocation to reproduction; allocation to sexual 74 reproduction rather than vegetative reproduction is critical for post-fire seedling recruitment, 75 dioecy is common and the fitness of co-occurring dioecious and hermaphroditic taxa can be 76 compared. Also, sexual dimorphism in the genus Leucadendron (Proteaceae) can be extreme 77 at a global scale. 78 The fynbos environment 79 Leucadendron contains about 80 species and occurs in fire-prone Cape (South Africa) 80 vegetation known as fynbos (sensu Rebelo et al. 2006). The Proteaceae dominate the fynbos 81 canopy layer which is about 2 m tall, mainly through the genera Protea and Leucadendron. 82 The family (about 360 fynbos species) includes both dioecious (25%) and hermaphroditic 83 taxa and which frequently co-exist Figure 1). Most Proteaceae species are reseeders (i.e. non- 84 resprouters) (Le Maitre and Midgley 1992). Since reseeders cannot resprout, all plants die in 85 fires. As they are relatively short-lived (1-3m tall, 5-30 years), plants also die in senescent 86 vegetation which occurs in the prolonged absence of fire (Bond 1980). Successful 87 recruitment of reseeders only takes place after a fire (Bond et al. 1987; Le Maitre and 88 Midgley 1992). About 60% of fynbos Proteaceae species are serotinous (Le Maitre and 89 Midgley 1990). When serotinous cones dry-out and open after death of adults in fire, seeds 90 are released en masse into the optimum post-fire environment where seedling recruitment 91 takes place in situ Figure 2). The most common soil seed-bank (35% of fynbos Proteaceae 92 species) is due to ant burial of seeds (Slingsby and Bond 1985; Le Maitre and Midgley 1992) 93 and most of remaining 5% of species have seeds that are scatter-hoarded by small mammals bioRxiv preprint doi: https://doi.org/10.1101/212555; this version posted November 1, 2017. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. 5 94 (Midgley and Anderson 2005). Species with soil seed-banks also germinate after fire as do 95 serotinous species; except in this case typically fire is needed to crack their relatively thick 96 seed coats. All three of these types of seed-stores occur in Leucadendron. 97 Given that only fires create suitable opportunities for regeneration, there is no strong 98 selection in fynbos for long distance seed dispersal such as by birds (Le Maitre and Midgley, 99 1992).
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