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Sexual Morph Specialisation in a Trioecious Nematode Balances Opposing bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-NC-ND 4.0 International license. 1 Title: Sexual morph specialisation in a trioecious nematode balances opposing 2 selective forces. 3 4 Authors: Sally Adams1*, Prachi Pathak1,2, Maike Kittelman3, Alun R.C. Jones4, 5 Eamonn B. Mallon4 and Andre Pires-daSilva1 6 7 8 Affiliations: 9 10 1 School of Life Sciences, University of Warwick, Coventry CV4 7AL, UK. 11 2 Institute of Cancer Sciences and Genomics, University of Birmingham, Birmingham, 12 B15 2TT, UK. 13 3 Department of Biological and Medical Sciences, Oxford Brookes University, 14 Headington Campus, Oxford, OX3 0BP, UK. 15 4 Department of Genetics and Genome Biology, University of Leicester, University 16 Road, Leicester, LE1 7RH, UK. 17 18 * Corresponding author ([email protected]) 19 20 Total word count 21 22 23 1 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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 The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity.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-NC-ND 4.0 International license. 24 ABSTRACT 25 The coexistence of different mating strategies, whereby a species can reproduce both 26 by selfing and outcrossing, is an evolutionary enigma that has long intrigued biologists 27 (Darwin, 1877). Theory predicts only two stable mating states : outcrossing with strong 28 inbreeding depression or selfing with weak inbreeding depression. As these two 29 mating strategies are subject to opposing selective forces, mixed breeding systems 30 are thought to be a rare transitory state, yet they have been found to persist even after 31 multiple speciation events. We hypothesise that if each mating strategy plays a 32 distinctive role during the species life history, opposing selective pressures could be 33 balanced, permitting the stable co-existence of selfing and outcrossing sexual morphs. 34 In this scenario, we would expect each sexual morph to be specialised in their 35 respective roles. Here we show, using a combination of behavioural, physiological and 36 gene expression studies, that the selfing (hermaphrodite) and outcrossing (female) 37 sexual morphs of the trioecious nematode Auanema freiburgensis have distinct 38 adaptations optimised for their different roles during the life cycle. A. freiburgensis 39 hermaphrodites are produced under stressful conditions, are specialised for dispersal 40 to new habitat patches and exhibit metabolic and intestinal changes that enable them 41 to meet the energetic cost of dispersal and reproduction. In contrast, A. freiburgensis 42 females are produced in favourable conditions, facilitate rapid population growth and 43 compensate for the lack of reproductive assurance by reallocating resources from 44 intestinal development to robust mate-finding behaviour. The specialisation of each 45 mating system for their role in the life cycle could balance opposing selective forces 46 allowing the stable maintenance of both outcrossing and selfing mating systems in A. 47 freiburgensis. 48 2 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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-NC-ND 4.0 International license. 49 50 51 52 3 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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-NC-ND 4.0 International license. 53 INTRODUCTION 54 Natural selection has driven the evolution of diverse modes of reproduction, 55 ranging from species that replicate exclusively from a single parent to those that have 56 separate sexes. The coexistence of different mating strategies within a species, where 57 conspecifics can reproduce either by outcrossing (male and female) or self-fertilising 58 (hermaphrodites), is an evolutionary enigma that has long intrigued biologists (Darwin, 59 1877). Species with such mixed mating strategies are usually considered a temporary 60 transitional state, as theory predicts only two stable mating states: outcrossing with 61 strong inbreeding depression or selfing with weak inbreeding depression 62 (Charlesworth, 1984; Charlesworth et al., 1990; Lande and Schemske, 1985). Yet 63 mixed breeding have been found to persist even after multiple speciation events 64 (Weeks, 2006), suggesting that in some cases they are not transitory. 65 Mixed mating strategies are expected to be rare, as they are subject to 66 opposing selective forces. In a transitory system, self-fertilising hermaphrodites should 67 outcompete females and males if there is strong selection for reproductive assurance 68 (guaranteeing reproduction even if a male is not available) (Pannell, 1997a; Wolf & 69 Takebayashi, 2004). Otherwise, dioecy (females and males) should dominate if 70 selection for reproductive assurance is relaxed, e.g. to reduce inbreeding or in 71 response to selection for sexual morph specialization, reviewed in (Charlesworth, 72 1999). We would expect a stable mixed mating system to exist only where these 73 opposing selective forces are balanced. 74 To date, the study of sexual polymorphisms has primarily focused on flowering 75 plants. However, the large and diverse phylum Nematoda provides an opportunity to 76 study the evolution and potential stability of mixed mating strategies and its 77 relationship to specific life histories. Although dioecy is the most common mode of 4 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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-NC-ND 4.0 International license. 78 reproduction in nematodes, several other mating systems have evolved, including 79 hermaphroditism, androdioecy (males and hermaphrodites) and trioecy (males, 80 females and hermaphrodites) (Denver et al., 2011; Pires-daSilva, 2007). The recently 81 described nematode genus Auanema (Kanzaki et al., 2017) displays trioecy, having 82 two egg-laying reproductive modes that coexist in a population: females, which must 83 outcross with males to reproduce, and hermaphrodites, which although able to cross 84 with males, predominantly reproduce by self-fertilisation (Tandonnet et al., 2018). 85 In A. freiburgensis, sex determination between non-males (females and 86 hermaphrodites) and males is regulated chromosomally: males inherit a single X 87 chromosome (XO), whilst hermaphrodites and females inherit two (XX) (Figure 1). 88 Auanema males are under-represented in populations, as they are produced at low 89 percentages both from male-female crosses (< 20%) and self-fertilising 90 hermaphrodites (< 10%) (Chaudhuri et al., 2015; Félix, 2004; Kanzaki et al., 2017; 91 Shakes et al., 2011; Winter et al., 2017). In contrast, environmental cues play an 92 important role in determining the non-male sexual morphs in A. freiburgensis (Robles 93 et al., 2021; Zuco et al., 2018). Whereas at low population density hermaphrodites 94 produce mostly female progeny, sensing of a crowding signal triggers the 95 hermaphrodite mother to switch to produce predominantly hermaphrodite offspring. 96 The female and hermaphrodite exhibit different larval development (Figure 1). When 97 in well-fed conditions at 20 °C, a hermaphrodite takes approximately 3 days from 98 hatching to adulthood. The hermaphrodite obligatorily passes through the dauer stage, 99 a specialised non-feeding, stress-resistant, migratory larva. In contrast, the A. 100 freiburgensis female and male never pass through dauer and reach adulthood after 101 approximately 2 days at 20 °C. 5 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 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-NC-ND 4.0 International license. Uncrowded Crowded (e.g new habitat patch) (e.g. old habitat patch) Uncrowded Crowded Mother Mother X0 XX XX Egg Egg Egg L1 L1 L1 s y a L2 L2 L2d d 2 ~ L3 L3 * s y a d migratory 3 L4 L4 dauer ~ X Adult Adult Crowding signal Male Female Progeny produced by outcrossing L4 Crowding signal Adult Hermaphrodite Progeny produced by self-fertilisation** 102 103 Figure 1 The life cycle of A. freiburgensis. 104 In A. freiburgensis, whether a mother produces females or hermaphrodite progeny depends upon her 105 perception of her habitat. In uncrowded conditions (blue arrows), she produces outcrossing female 106 progeny, but upon sensing a crowding signal can switch to producing selfing hermaphrodites (red 107 arrows). Hermaphrodite progeny pass through an obligatory dauer larval stage optimised for migration. 108 If dispersed to a new habitat patch the dauer will complete reproductive development and produce 109 progeny by self-fertilisation. If this new habitat patch is uncrowded the hermaphrodite will produce 110 mostly female (and male) progeny (blue arrows). As neither females or males pass through the dauer 111 diapause larval stage they reach sexual maturity quicker, which could allow more rapid population 112 growth in new habitats. Times for development are based on well fed conditions at 20°C. *The dauer 6 bioRxiv preprint doi: https://doi.org/10.1101/2021.08.31.458370; this version posted September 1, 2021.
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