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Definition of Sex Based on Reproductive Cells Short Title 1 Definition of sex based on reproductive cells 2 Short title: Cell-based definition of sex 3 Zhongneng Xu*1, 2 4 5 * --corresponding author, [email protected]; [email protected] 6 7 1Department of Ecology, Jinan University, Guangzhou 510632, China; 2Department of 8 Aquatic Bioscience, GraduateSchool of Agricultural and Life Science, the University 9 of Tokyo, Tokyo 113-8657, Japan. 10 Abstract 11 Increasing evidence shows that sex in some organisms, including humans, is a 12 continuous spectrum and sometimes, sexual differences in the organs of an individual 13 are contradictory and affected by physiological, pathological, and environmental 14 factors. The current definition of sex is thus in question. The present study indicated 15 that the definition of sex based on individuals, especially in multicellular organisms, is 16 inappropriate because the essence of sex was to distinguish between reproductive 17 subjects and the unit of reproduction is not an individual but a gamete cell. A definition 18 of sex based on gamete cells was thus proposed, focusing on material contributions 19 to reproduction by gamete cells and the formation of totipotent cells. To make this 20 definition of sex compatible with current related knowledge systems, individual sex 21 based on the quantitative proportions of different germ cells was also defined. The 22 relationships between the cell-based definition of sex and sex determination, sex 23 differences, and gender equality were discussed. 24 25 Word count = 155 26 Keywords = definition of sex, germ cell, reproduction, sex determination, sex 27 differences 28 1 Introduction 29 “Sex" has two meanings, sexual reproduction and gender, and in the present 30 study it refers to the latter. There has been a long history since sex was taken as an 31 academic issue. In his famous work Politics, Aristotle describes in detail human beings 32 born with different sexes (Jowett, 1885). The struggle for sex competition and sex 33 equality in human society is arduous. A sexually mature animal can accurately identify 34 the opposite sex, start its pursuit, and initiate a mating offensive. Biologists and 35 sociologists often consider sex differences when conducting research. All these show 36 that sex is a biological, social, and philosophical issue. The starting point for these 37 questions is: What is sex? The answer seems to be a common sense that cannot be 38 questioned, but it is actually full of many possibilities and exceptions. Social laws, 39 moral standards, academic authorities, social organizations, and governments may 40 impede the researchers' further thoughts of breaking through the current definition of 41 sex. However, some objective problems are increasingly plaguing scientists’ and 42 ordinary people's views on sex. These include both biological problems, such as the 43 parasex phenomenon of somatic cells (Pontecorvo, 1956) and male parthenogenesis 44 of plants and animals (Davies, 1958; Li et al., 2018), and social problems, such as the 45 phenomenon of intersex and homosexuality. This has to make us think more deeply 46 again: What is sex? 47 48 2 Confusion of the current definition of sex 49 Sex is a vital feature of sexually reproductive organisms. It is relevant to the 50 study of biological phenomena and, more importantly, is one of the indexes in diverse 51 human management systems. The current definition of sex is based on individuals, 52 involving reproductive functions, reproductive systems, genetic markers, etc. (Purves 53 et al, 2000; Knox and Schacht, 2011; Stevenson and Waite, 2011) ， and some 54 researchers broadly viewed sex as the feature in mixing genetic materials from 55 different individuals to form new individuals (Colegrave, 2012). Why the unit of sex in 56 the current definition of sex is based on individual is unclear, but at least from the 57 perspective of human sensory perception, differences in the appearances of human 58 individuals, as well as many other species, can indicate differences in reproductive 59 function. 60 Individuals of single-cell organisms are cells, so the unit of sex in unicellular 61 organisms is both an individual and a cell. The situation of multicellular organisms, 62 which is focused in the present study, is complicated. Individuals of multicellular 63 organisms are usually identified as females, males, or hermaphrodites according to 64 organ differences, gamete production, and sex chromosomes. Perhaps sex glands are 65 the major indexes to anatomically discriminate between males and females, and 66 external genitalia are another suitable candidate that does not require a bio-assay, 67 especially from the perspectives of the layperson. However, hermaphroditic individuals 68 are found among dioecious species, and some dioecious species, including humans, 69 even exhibit a continuous spectrum of phenotypes between females and males, 70 especially in the cases of some genetic and chromosomal diseases (Blackless et al., 71 2000; Matson et al, 2011; Ainsworth, 2015). Gonad primordia in embryos have the 72 plastic potential to develop into female gonads or male gonads (Wilhelm et al., 2007). 73 With respect to external genitalia, surgical operations can change the sex of human 74 individuals of both male-to-females and female-to-males (Dhejne et al., 2011). Other 75 organs also have sex differences, including the brain. The sex of the brains is a 76 contested issue in biology and social management, and the sex of the brain sometimes 77 contradicts the sex shown by sexual chromosomes, sexual glands, and external 78 genitalia (Rogers, 2002). In some societies, gender is decided by self-recognition, and 79 a difference between personally-recognized sex and phenotypic sex is acceptable. 80 Identifying sex by on the basis of sex chromosomes is increasingly questioned. The 81 phenomenon of sex chromosome mosaicism has been demonstrated, and cells from 82 male embryos can be detected in the blood of their mothers (Hotta and Benzer, 1972; 83 Erlebacher and Fisher, 2017). More perplexingly, under some conditions, e.g., 84 biotechnological operations, stem cells in vitro can change into eggs and sperms 85 (Hayashi et al., 2012; Irie et al., 2015; Saitou and Miyauchi, 2016). 86 Obviously, it is not sex that is confused, but the definition of sex. The present 87 paper addresses a proposal to confirm a definition of sex based on the essentially 88 biological significance of sex. 89 90 3 The essential nature of sex 91 Sex is dependent on sexual reproduction. The significance of sex lies in the 92 biological process of reproduction, especially in the period of fertilization and zygote 93 development in eukaryotes. Unlike asexual reproduction, sexual reproduction involves 94 the melding of two gametes and the sharing of the genetic materials. This process is 95 believed to be beneficial to genetic diversity of offspring, although whether the genetic 96 diversity allows them to adapt to the environment is another question (Kondrashov, 97 1993; Gross, 1996; Otto and Whitton, 2000). During fertilization, the gametes must be 98 distinguished from each other. In primitive isogamous organisms, the gametes are 99 difficult to be distinguished. In these species, “mating type”, an analogue of “sex”, is 100 used to describe the different groups that can mate. For anisogamous organisms, sex 101 is used to distinguish the highly differentiated gametes. Zygotes receive not only 102 genetic materials but also nutrients and organelles from the gametes. Thus, the 103 concept of sex should carry information about the contribution of genetic materials, 104 nutrients, and organelles from the gametes. 105 In sexual reproduction, individual organisms are the donors of germ cells, but 106 only germ cells are involved in the biological processes of sexual reproduction, such 107 as meiosis and fertilization. Germ cells of unicellular organisms and some multicellular 108 organisms proceed the syngamy in the external environment. Some species with 109 sexual reproduction have special passages for sperms and eggs and special sites for 110 the development of fertilized eggs, and these organs, such as the penis, the vagina, 111 and the uterus, are often the criteria used to define the sexes of individuals. 112 Considering all species with sexual reproduction, however, the commonality of the birth 113 of new life is fertilization, not the combination of individuals or the specific reproductive 114 organs. That is, the unit of sexual reproduction is not the individual, but the germ cell. 115 Sex should thus describe the characteristics of the germ cells. Therefore, a definition 116 of sex that is suitable for all species with sexual reproduction must be based on cells, 117 not individuals. 118 Some people think that prokaryotes and viruses can reproduce sexually 119 because recombination of genetic materials in these organisms are found. However, 120 this raises the arguments about the definition of sexual reproduction in eukaryotes and 121 prokaryotes. Obviously, there is the concept of eukaryotic sexual reproduction first in 122 history, and the phenomenon of genetic recombination in eukaryotic sexual 123 reproduction is an important discovery in modern biology. Taking recombination as the 124 dentification standards for sexual reproduction is to use the nature of (eukaryotic) 125 sexual reproduction to in turn define (prokaryotic) sexual reproduction, which is a 126 problem of circular argument. Some of these arguments are described below. This 127 argument does not affect the present study because prokaryotes and viruses are 128 single-cells or single-particles, and the unit of their reproduction is also cells (or single 129 virus particles), resulting in the cellular characteristics of the speculative sex in these 130 species. 131 132 4 Cell-based sex in the hypotheses of the origin of sexual reproduction 133 The origin of sexual reproduction is hypothesized in the ancestral prokaryotes 134 or ancestral eukaryotes according to different evolutionary biologists, but each 135 hypothesis uses single cells as the starting point for sexual units.
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