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Determining reproductive mode in Japanese harvesters: The search for sex.

**This post is a part of the series on the 2019 AGA Presidential Symposium – Sex and Asex: the genetics of complex life cycles**


About the author: Tyler Brown is a PhD candidate in Dr. Mercedes Burns’ lab at the University of Maryland, Baltimore County. His research focuses on sexual conflict and its role in the maintenance of geographic parthenogenesis in facultatively parthenogenetic harvesters. Tyler received his B.S. in Biological Sciences from the University of Maryland, College Park and can be found on twitter @NotASpider_.






Sexual reproduction is nearly ubiquitous in animals (de Visser & Elena 2007). Its benefits are well-documented, but that doesn’t mean there aren’t also significant costs to sex. These include the two-fold cost of males, the cost of meiosis, and the costs of mating (Lehtonen et al. 2012; Roze 2012). Females are more often than not the ones that suffer the consequences (Lehtonen et al. 2012). While sex may confer long-term, inclusive fitness benefits, asexuality is often more beneficial to females in the short-term (Becks & Agrawal 2012; Fiegal et al. 2009). So, why is sex so common?

This is the paradox of sex.

Given its myriad costs, 99% of animal species still reproduce sexually. The magnitude of the benefits must be particularly strong.

To better understand this paradox, the study of alternative reproductive modes, such as asexuality, is necessary.

Leiobunum manubriatum and L. globosumare a pair of facultatively parthenogenetic harvesters (commonly known as daddy-long-legs) native to central and northern Japan. Males have morphological features indicative of sexual conflict-their clasping pedipalps are significantly larger than female pedipalps (Burns et al. 2017). Some populations also display extreme female-biased sex ratios, with males being rare or nonexistent in the northernmost populations. Thus, harvesters display geographic parthenogenesis where asexuals (or parthenogens) are more common in marginal habitats, suggesting that facultatively and obligately parthenogenetic species might be better suited for these marginal habitats than obligately sexual species (Kearney 2005).

As shown in theoretical modeling by Gerber and Kokko (2016) and Burke and Bonduriansky (2018), sexual conflict can play a significant role in maintaining geographic parthenogenesis in facultatively parthenogenetic species. To better understand the role of sexual conflict in our own focal species, our study (Brown et al. 2020) set out to answer two basic questions: dofacultatively parthenogenetic females mate? And if so, where?

To answer these questions, we collected adult females of L. manubriatum (Figure 1) and L. globosum, as well as two closely related, obligately sexual species, L. tohokuense and L. curvipalpe, in 2015 and 2016. After maintaining the females and collecting any oviposited eggs, we employed three sequencing methods to determine the reproductive mode. MassArray SNP genotyping and 3RAD sequencing were used for the 2015 samples, while 3RAD-Capture, which consists of a 3RADseq protocol followed by a bait capture protocol, was used for the 2016 samples. Baits for the bait capture protocol were developed from the 2015 sequencing results, which allowed us to “target” specific regions of the genome to maximize our usable reads for genotyping.

Figure 1: Mating pair of Leiobunum manubriatum (female lower left with dark stripes, male upper right) on mossy rock in Toyama Prefecture, Japan. Photo taken by Dr. Sarah Stellwagen and published in Brown et al. (2020).

We used several methods to determine reproductive mode. We measured the heterozygosity of the dams and offspring, the rate of transition (T) from homozygous dam loci to heterozygous offspring loci, and the clone probability as calculated by Colony. A high Tand low average clone probability would indicate sexual reproduction, while asexual reproduction would be indicated by a low Tand high average clone probability. Due to the rarity of males in the north, we expected to see evidence of more frequent asexual reproduction in these populations. Conversely, common males in the south led us to expect a high frequency of sexual reproduction.

We found that asexual reproduction is likely the primary mode of reproduction in the female-biased northern populations, however, it is still unclear whether this is due geographic factors favoring parthenogens or female resistance to male mating attempts (sexual conflict). Despite males being more common in southern populations, we found that sexual reproduction was still less prevalent than expected. This may be due to southern females being locally adapted to male presence and harassment, potentially allowing them to better resist mating attempts and avoid the associated costs. We plan to further investigate the role of sexual conflict over reproductive mode and mating rate in these harvesters. We also hope to further investigate the factors responsible for the maintenance of sex and geographic parthenogenesis in the unique study system of L. manubriatumand L. globosum as a whole. Because sex is nearly ubiquituous in animals, alternative reproductive systems in which sex is not obligatory should be particularly useful in the study of the paradox of sex.

Becks, L., & Agrawal, A. F. (2012). The evolution of sex is favoured during adaptation to new environments. PLoS Biology, 10(5).

Brown, T. A., Tsurusaki, N., & Burns, M. (2020). Genomic Determination of Reproductive Mode in Facultatively Parthenogenetic Opiliones. Journal of Heredity, esaa045.

Burke, N. W., & Bonduriansky, R. (2018). The geography of sex: Sexual conflict, environmental gradients and local loss of sex in facultatively parthenogenetic animals. Philosophical Transactions of the Royal Society B: Biological Sciences, 373(1757).

Burns, M., Hedin, M., & Tsurusaki, N. (2017). Population genomics and geographical parthenogenesis in Japanese harvestmen (Opiliones, Sclerosomatidae, Leiobunum).Ecology and Evolution, 8(1), 36–52.

de Visser, J. A. G. M., & Elena, S. F. (2007). The evolution of sex: empirical insights into the roles of epistasis and drift. Nature Reviews Genetics, 8(2), 139–149.

Feigel, A., Englander, A., & Engel, A. (2009). Sex is always well worth its two-fold cost. PloS One, 4(7), e6012.

Gerber, N., & Kokko, H. (2016). Sexual conflict and the evolution of asexuality at low population densities. Proceedings of the Royal Society B: Biological Sciences, 283(1841), 20161280.

Kearney, M. (2005). Hybridization, glaciation and geographical parthenogenesis. Trends in Ecology & Evolution, 20(9).

Lehtonen, J., Jennions, M. D., & Kokko, H. (2012). The many costs of sex. Trends in Ecology and Evolution, 27(3), 172–178.

Roze, D. (2012). Disentangling the Benefits of Sex. PLoS Biology, 10(5), e1001321.

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