The Evolutionary History of Sexual Systems in Fish
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bioRxiv preprint doi: https://doi.org/10.1101/2021.01.25.428070; this version posted January 26, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 1 Switches, stability and reversals: 2 the evolutionary history of sexual systems in fish 3 4 5 6 Susanna Pla1#, Chiara Benvenuto2#, Isabella Capellini3* & Francesc Piferrer1* 7 8 9 10 ¹Institut de Ciències del Mar, Spanish National Research Council (CSIC), Barcelona, Spain 11 2School of Science, Engineering and Environment, University of Salford, Salford, UK 12 3School of Biological Sciences, Queen’s University Belfast, UK 13 14 #Joint first authors 15 16 17 *Correspondence: Dr. Francesc Piferrer, Institut de Ciències del Mar, Spanish National 18 Research Council (CSIC), Passeig Marítim, 37-49, 08003 Barcelona. Tel. +34-932 309 567; 19 E-mail: [email protected] 20 21 *Correspondence: Dr. Isabella Capellini, School of Biological Sciences, Queen’s University 22 Belfast, 19 Chlorine Gardens, Belfast, BT9 5DL, Northern Ireland, United Kingdom; E-mail: 23 [email protected] 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.25.428070; this version posted January 26, 2021. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-ND 4.0 International license. 24 Abstract 25 26 Sexual systems are highly diverse and have profound consequences for population dynamics 27 and resilience. Yet, little is known about how they evolved. Using phylogenetic Bayesian 28 modelling on 4740 species, we show that gonochorism is the likely ancestral condition in 29 teleost fish. While all hermaphroditic forms revert quickly to gonochorism, protogyny and 30 simultaneous hermaphroditism are evolutionarily more stable than protandry. Importantly, 31 simultaneous hermaphroditism can evolve directly from gonochorism, in contrast to theoretical 32 expectations. We find support for predictions from life history theory that protogynous species 33 live longer than gonochoristic species, are smaller than protandrous species, have males 34 maturing later than protandrous males, and invest the least in male gonad mass. The large-scale 35 distribution of sexual systems on the tree of life does not seem to reflect just adaptive 36 predictions and thus does not fully explain why some sexual forms evolve in some taxa but not 37 others (William’s paradox). We propose that future studies should take into account the 38 diversity of sex determining mechanisms. Some of these might constrain the evolution of 39 hermaphroditism, while the non-duality of the embryological origin of teleost gonads might 40 explain why protogyny predominates over protandry in this extraordinarily diverse group of 41 animals. 42 43 44 Keywords 45 Hermaphroditism, phylogeny, Williams’ paradox, Dollo’s law, developmental plasticity, sex 46 determination 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.25.428070; this version posted January 26, 2021. 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-ND 4.0 International license. 47 Introducction 48 49 Sexual reproduction is a unifying feature of Eukaryotes1 and yet it is extremely diverse2. 50 Sexual systems, defined as the distribution of the male and female function among the 51 individuals of a given species, vary from separate fixed sexes (known as gonochorism in 52 animals and dioecy in plants) to simultaneous hermaphroditism (each individual produces both 53 male and female gametes at the same time). These two sexual systems can be viewed as the 54 extremes in a sexually plastic gradient3 of intermediate (sequential hermaphroditism) and 55 mixed (coexistence of males and/or females with hermaphrodites)4,5 systems. Sexual systems 56 have a profound influence on individuals’ mating success and fitness6, population sex ratios 57 and effective sizes7, and colonization events and habitat use8. As a result, sexual system 58 influence the population dynamics and resilience to natural and anthropogenic stressors of 59 ecologically and commercially important species that are often endangered or overexploited9. 60 Hermaphroditism is predominant in flowering plants, i.e., angiosperms10, where 94% 61 of the species have male and female sex organs in the same individual/flower, and it is 62 widespread in invertebrates and fish, totalling 5% of animal species or up to ~30% if insects 63 are excluded11. While this diversity suggests multiple evolutionary transitions between sexual 64 systems in response to selection, current evolutionary models on the adaptive advantage of 65 different sexual systems explain little about how and why sexual systems evolve and thus their 66 large-scale distribution across the tree of life (Williams’ paradox4,12). Thus, unravelling the 67 evolutionary history of sexual systems and quantifying how frequently and in what direction 68 transitions occur, is key to revealing which sexual systems are evolutionarily labile or stable, 69 elucidating how one changes into another over evolutionary time, and identifying the 70 environmental, genetic and developmental drivers favouring or opposing these changes. Yet, 71 our understanding of how sexual systems evolve is still limited, particularly in animals. 72 Theoretical models, initially developed for plants, suggest that simultaneous 73 hermaphroditism and dioecy are evolutionary stable conditions that are retained over long 74 evolutionary time and unlikely lost once evolved, while mixed sexual systems represent 75 evolutionary intermediate stages4,5,13 (Fig. 1). 76 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.25.428070; this version posted January 26, 2021. 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-ND 4.0 International license. 77 78 79 Fig. 1. Theoretical framework for the evolution of sexual systems: potential evolutionary 80 transitions between gonochorism and simultaneous hermaphroditism via mixed systems 81 (mixed pathways) as described in plants and some animals; via sequential hermaphroditism 82 (sequential pathways) as recently suggested4; or without intermediate states (direct pathways) 83 as proposed for plants6. Double-headed arrows indicate theoretical pathways. Large arrows 84 identify the directionality more frequently investigated for plants (green) and animals (blue), 85 from the most common to the rarest state. 86 87 88 Simultaneous hermaphroditism is likely the ancestral state in angiosperms from which 89 dioecy, a rare sexual system in plants6, has evolved independently several times, possibly to 90 avoid inbreeding14,15. Theoretical models predict that separate sexes in plants evolve from 91 hermaphroditism in different ways: 1) primarily through the intermediate state of gynodioecy16, 92 a sexual system common in plants that occurs when a male-sterile mutant invades an 93 hermaphroditic population resulting in the coexistence of hermaphrodites and females; 2) 94 androdioecy, where the mutation results in female sterility, resulting in the coexistence of 95 hermaphrodites and males, which is less common in plants17,18; 3) possibly via trioecy, i.e., the 96 coexistence of hermaphrodites, males and females, which is very rare; and 4) less frequently, 97 via a direct transition6,10 (Fig. 1). However, in animals no evidence of a direct transition exists. 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.01.25.428070; this version posted January 26, 2021. 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-ND 4.0 International license. 98 Once gained, dioecy was believed to be an irreversible condition19, a conclusion based on the 99 assumption that returning to a simultaneous expression of male- and female-specific genes 100 would likely produce contrasting effects on sex-specific physiology. Recent studies, however, 101 reject this claim in plants, as phylogenetic reconstructions of direct transitions from 102 dioecy/gonochorism to simultaneous hermaphroditism have been documented10,20. 103 The same theoretical framework with mixed pathways has been proposed also for 104 animals where, in contrast to plants, gonochorism is the most common sexual system, 105 androdioecy is more common than gynodioecy5,13 and trioecy is very rare21. However, several 106 reproductive characteristics in plants are quite different from the ones evolved in animals22, 107 albeit similarities can be found in some invertebrates23; hence, different theoretical frameworks 108 are required (Fig. 1). Furthermore, evolutionary transitions between sexual systems in fish, the 109 only vertebrates to exhibit hermaphroditism24, might be less likely to occur preferentially via a 110 mixed pathway (Fig. 1) given that in fish (>30000 species) only a few killifish species in the 111 genus Krytpolebias (formerly Rivulus) are truly androdioecious5,25,26 while the presence of 112 gynodioecy and trioecy is