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Mating-Induced Male Death and Pheromone Toxin-Regulated Androstasis

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Mating-Induced Male Death and Pheromone Toxin-Regulated Androstasis bioRxiv preprint first posted online Dec. 15, 2015; doi: http://dx.doi.org/10.1101/034181. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. Shi, Runnels & Murphy – preprint version –www.biorxiv.org Mating-induced Male Death and Pheromone Toxin-regulated Androstasis Cheng Shi, Alexi M. Runnels, and Coleen T. Murphy* Lewis-Sigler Institute for Integrative Genomics and Dept. of Molecular Biology, Princeton University, Princeton, NJ 08544, USA *Correspondence to: [email protected] Abstract How mating affects male lifespan is poorly understood. Using single worm lifespan assays, we discovered that males live significantly shorter after mating in both androdioecious (male and hermaphroditic) and gonochoristic (male and female) Caenorhabditis. Germline-dependent shrinking, glycogen loss, and ectopic expression of vitellogenins contribute to male post-mating lifespan reduction, which is conserved between the sexes. In addition to mating-induced lifespan decrease, worms are subject to killing by male pheromone-dependent toxicity. C. elegans males are the most sensitive, whereas C. remanei are immune, suggesting that males in androdioecious and gonochoristic species utilize male pheromone differently as a toxin or a chemical messenger. Our study reveals two mechanisms involved in male lifespan regulation: germline-dependent shrinking and death is the result of an unavoidable cost of reproduction and is evolutionarily conserved, whereas male pheromone-mediated killing provides a novel mechanism to cull the male population and ensure a return to the self-reproduction mode in androdioecious species. Our work highlights the importance of understanding the shared vs. sex- and species- specific mechanisms that regulate lifespan. Keywords: Caenorhabditis, mating, pheromone, death Introduction C. remanei, 50% of the population is male, and females and males must mate to reproduce. The mating efficiency of C. The interplay between the sexes influences an individual’s elegans males is very low compared to C. remanei males8. longevity1-3. Caenorhabditis female lifespan is shortened after 4 Gonochoristic species females secrete pheromones that attract mating through receipt of male sperm and seminal fluid , and 10 5 males , and have distinct behaviors during mating compared separately by exposure to male pheromone . However, to hermaphrodites11,12. How males in androdioecious and previous studies reported contradictory results on how mating 3,6 gonochoristic species cope with these different mating influences male lifespan . Therefore, whether and how male situations remains poorly understood. Moreover, the utility of lifespan is affected by prolonged exposure and interactions killing females by exposure to male pheromone in with females is largely unknown. gonochoristic populations5 is unclear. The Caenorhabditis genus consists of both androdioecious Here we report that after mating, Caenorhabditis males suffer (male and hermaphroditic) and gonochoristic (male and from germline-dependent shrinking and death, just as in the female) species. In androdioecious species such as C. elegans, case of mated C. elegans hermaphrodites and C. remanei the population is dominated by hermaphrodites, which females4. However, C. elegans males and hermaphrodites reproduce by self-fertilization. Males are usually very rare have differential sensitivity to male pheromone-dependent (less than 0.2% for the standard lab strain N2) and are toxicity, while C. remanei seem immune to this toxicity, and produced due to spontaneous X chromosome 7,8 instead use sex-specific pheromones to identify mates. Thus, nondisjunction . Under stressful conditions, more oocytes androdioecious and gonochoristic species differentially utilize experience chromosome non-disjunction, thus androdioecious pheromone for mating vs hermaphroditic maintenance, while species periodically undergo explosions of male populations. both species suffer the cost of mating through germline- The existence of males in androdioecious species may reduce dependent shrinking and death. inbreeding and facilitate adaptation to changing environments9. By contrast, in gonochoristic species such as 1 bioRxiv preprint first posted online Dec. 15, 2015; doi: http://dx.doi.org/10.1101/034181. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. Shi, Runnels & Murphy – preprint version –www.biorxiv.org Results ~35% compared with the unmated solitary males (Fig. 1A, Table S1), similar to the lifespan decrease of mated C. elegans males live shorter after mating hermaphrodites4. Also like females, males shrank after 6 days’ C. elegans hermaphrodites shrink up to 30% and live 40% mating; by Day 7, the mated males were 10% smaller than the shorter after mating4. We wondered if males also experience unmated solitary males control (Fig. 1B,C, Table S2). such extreme post-mating changes. Traditional lifespan assays Males die faster when paired with a hermaphrodite for a are performed using grouped worms; however, grouped males longer period: mating with a hermaphrodite for one day did live shorter than solitary males13, which could mask the not affect the lifespan of the male, while 2-3 days’ mating lifespan shortening effect of mating in males. Therefore, we shortened male lifespan by 15%, 4-5 days’ mating reduced measured the lifespans of solitary males and single males their lifespan by 25%, and 6 days’ mating increased the paired with a single hermaphrodite for 6 days from Day 1 to reduction to over 35% (Fig. 1D). By contrast, the number of Day 6 of adulthood. (We used fog-2(q71) worms in our assay; hermaphrodites paired with the single male during mating had fog-2 males are equivalent to wild-type (N2) males, while fog- much less effect compared to mating duration (Fig. 1E, Fig. 2 hermaphrodites are self-spermless14, enabling identification S1A,B). The time at which mating occurs within the of successful mating.) Mated male lifespan was decreased reproductive period is also not critical for males’ post-mating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igure 1. C. elegans males shrink and die early after mating. 2 bioRxiv preprint first posted online Dec. 15, 2015; doi: http://dx.doi.org/10.1101/034181. The copyright holder for this preprint (which was not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission. Shi, Runnels & Murphy – preprint version –www.biorxiv.org lifespan decrease; given the same mating duration, males Elevated germline proliferation is one of the major causes of mated with hermaphrodites for the first three days of hermaphrodites’ early death after mating4. We wondered adulthood had a similar lifespan decrease as those mated with whether this killing mechanism is conserved in males. Adult hermaphrodites during Days 6-8 of adulthood (Fig. 1F). treatment with the DNA replication inhibitor 5- fluorodeoxyruridine (FUdR) has little effect on lifespan and meiosis at low dosage (50 !M)16, but rapidly blocks germline C. elegans males’ post-mating shrinking and death are 4 germline-dependent proliferation in mated hermaphrodites . When treated with 50!M FUdR during the three-day mating period, male We wondered whether pheromone is required for mating- lifespan was unchanged (Fig. 2C). FUdR treatment also induced death in males. To distinguish pheromone from a eliminated male post-mating lifespan decrease in our 6 days’ direct mating effect, we tested daf-22(m130) mutants, which mating regime (Fig. S1C,D). Additionally, lacking the are deficient in ascaroside pheromone biogenesis15. Wild-type germline prevented both shrinking and death: mating caused males still died early post-mating when paired with a daf-22 neither shrinking nor lifespan decrease in germline-less glp- hermaphrodite for 6 days (Fig. 2A). Likewise, daf-22 mutant 1(e2141) males (Fig. 2D,E, Fig. S1E). These results suggest males lived shorter after 6 days’ mating (Fig. 2B), indicating that germline-mediated post-mating lifespan regulation is that the post-mating lifespan decrease in our single-worm pair conserved between sexes to a large extent. lifespan assay is due to mating itself rather than pheromone from either sex. A B #!! #!! #( !"#.$$%&'()*,#( '! #)#(*&+,)-!"#.$$ '! #+,.$@!"#.$$,#)#(*&+ &! &! %! %! 9:;<:=7,25;>?>06 $! 9:;<:=7,25;>?>06 $! ! ! ! " #! #" $! ! " #! #" $! $" /012,3),4+567833+ /012,3),4+567833+ C D #!! #!! #( ,-..',#( '! A)#(*A+ '! ,-..',#)#(*&+ A)#(*A+BCD+E*A+ &! &! %! %! 9:;<:=7,25;>?>06 $! 9:;<:=7,25;>?>06 $! 26 ˚C ! ! ! " #! #" $! ! " #! #" /012,3),4+567833+ Days of Adulthood E F '""" &#" &"" #!! #!! %#" *** %"" $#" "! "! Body length (µm) !"#$%&'(%)%*+/01)234 $"" !"#$%&'(%)%*+1)234 !#" G61<3F:=,H70?=?=F,I0J,5JK G61<3F:=,H70?=?=F,I0J,5JK ! ! !"" + + + 7:+ ()*+' ()*+, ()*+- ()*+. ()*+# ()*+! ()*+$ ,5=(0 ,(06: 26 ˚C )3F.$,(06:2,5=(07:)3F.$,(06:2,(07:+,"
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