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34667 U01 UNCORR PRF 1..14 34667_u01_UNCORR_PRF.3d_1_08-27-07 Part I Strategies, Methods and Background ____À1 ____0 ____þ1 34667_u01_UNCORR_PRF.3d_2_08-27-07 1 ____ 0 ____ 1 ____ 34667_u01_UNCORR_PRF.3d_3_08-27-07 Chapter 1 Why Are There Two Sexes? Turk Rhen and David Crews One of the most fascinating aspects of life on earth is underlying sexual differentiation of the body and the myriad of differences between males and females mind should lead to novel therapies designed to pre- (Judson, 2002). Children and adults alike are capti- vent birth defects and cure devastating neurological vated when they first learn that males, rather than diseases. females, gestate and give birth to offspring in certain To fully comprehend sex differences in the brain species of seahorse. Role reversal is also observed in and behavior in humans and to appreciate how ani- the red-necked phalarope, a shorebird in which poly- mals can be used to model these differences, we need androus females are more brightly colored than their to examine sexual dimorphisms in an evolutionary mates and males alone incubate eggs. People are like- context. The basic principle that guides biomedical wise amazed when they hear that ambient tempera- research is that genetic, developmental, physiological, ture determines the sex of many reptiles. While such and behavioral mechanisms are conserved in species unusual phenomena capture our curiosity, there are that have evolved from common ancestors. The unity also practical reasons for studying sex differences. For of life is seen in our hereditary material: the universal instance, defects in development of the reproductive genetic code, the enzymes that synthesize DNA, and tract and genitalia are fairly common in humans. Sex the proteins that distribute chromosomes to daughter differences in physiology and disease affect virtually cells during mitosis and meiosis. This principle also every organ system in the human body, including the permits significant advances in neuroscience. Hodg- nervous system. Depression, Alzheimer’s disease, and kin and Huxley, for example, used the giant axon of schizophrenia are examples of afflictions that differ squid to elucidate action potentials (Clay, 2005). Our in incidence, onset, and/or symptoms between males knowledge of the mechanisms underlying long-term ____À1 and females. Understanding of the mechanisms potentiation and learning has been furthered by studies ____0 ____þ1 3 34667_u01_UNCORR_PRF.3d_4_08-27-07 4 STRATEGIES, METHODS AND BACKGROUND in sea slugs (Kandel, 2004). Research on guinea pigs ultimately drives neural evolution. We bring the has been critical in formation of the concept of or- chapter to a close by briefly outlining what is known ganization and activation of sexual behavior by go- about sexual differentiation of neural mechanisms in nadal steroids (Pheonix et al., 1959). Consequently, humans. These mechanisms are undoubtedly related male seahorses giving birth, polyandrous female phal- to sex differences in aggressive and sexual behavior aropes, and reptiles with temperature-dependent sex and emotional memory, as well as the incidence of determination may not be as esoteric as they seem if affective disorders, anxiety disorders, schizophrenia, conserved genes and biological processes have been and post-traumatic stress disorder (PTSD). co-opted for different uses during evolution. Still, these examples highlight an emerging paradox in studies of sexual differentiation. Reproductive traits in THE EVOLUTION OF EUKARYOTES, general appear to be evolving more rapidly than other MEIOSIS, AND TWO SEXES characteristics. Here we provide a three-part intro- duction to sex differences, stressing both the conserved Advances in molecular and cellular biology, along and the unique as part of Darwin’s notion of descent with comparative genomics, are allowing reconstruc- with modification (Darwin, 1859). tion of the earliest stages in the evolution of life on In the first section, we step back in time and pro- earth. The first organisms lacked a membrane-bound vide a broad perspective on the evolution of eukary- nucleus, replicated by binary fission, and are survived otes. The evolution of meiosis and syngamy (i.e., the by today’s prokaryotes. Two groups of extant prokary- fusion of two cells) was a precondition for the evolu- otes, the eubacteria and the archaebacteria, appear to tion of dimorphic gametes and the subsequent evo- be as distinct from one another as they are from eu- lution of all other sex differences. We then outline karyotes (Brown & Doolittle, 1997; Bell & Jackson, general causes of sex differences in animals by fo- 2001; Forterre, 2001; Makarova & Koonin, 2003; cusing on natural and sexual selection. In particular, Robinson & Bell, 2005). This finding makes it diffi- we illustrate how sex-specific selection can favor dif- cult to codify the prokaryote-eukaryote transition (Mar- ferent phenotypes in males and females. This pattern tin, 2005). Yet, research is beginning to elucidate how of divergent selection ultimately leads to changes in the first nucleated cells originated and diversified. the neural mechanisms that regulate behavior in the Some of the most important events in the evolution of two sexes. eukaryotes involved symbioses (mutually beneficial In the second section, we explain the mechanisms associations of different species). For instance, the that underlie sex differences in gene expression as well endosymbiotic theory for the origin of mitochondria as the basic developmental mechanisms that produce is well established, even if the timing is in dispute sex differences. Despite abundant examples of differ- (Embley & Martin, 2006). ential selection on males versus females, there is an One hypothesis has it that the first eukaryotes inherent constraint to the evolution of sex differences. lacked endosymbionts (currently represented by di- To be precise, the same genes control homologous plomonads, parabasalids, and microsporidia) and that traits in both sexes. We describe how several mecha- endosymbionts were acquired in a separate lineage nisms relieve this genetic constraint. For instance, ge- that gave rise to eukaryotes with mitochondria. An netic differences in the form of sex chromosomes and alternative hypothesis suggests that endosymbiotic sex-linked genes have evolved independently in many bacteria were acquired concurrent (or nearly so) with eukaryotic lineages. Another major mechanism is sex- the origin of eukaryotes and that these organisms limited (or differential) expression of autosomal loci, evolved into mitochondria as well as the more derived as exemplified by hormonal regulation of gene expres- organelles called hydrogenosomes and mitosomes in sion. Environmental factors can also have a large im- eukaryotes that lack prototypical mitochondria (Em- pact on the development of sex differences, a pheno- bley & Martin, 2006). In either case, this ancient menon commonly referred to as phenotypic plasticity. event has direct implications for human health be- Finally, we review some elegant research that links cause mutations in mitochondrial DNA, which is evolutionary causes of and proximate mechanisms for maternally inherited, cause a number of diseases 1 ____ sex differences in the brain and behavior. These ex- (Chen & Butow, 2005; Dimauro & Davidzon, 2005). 0 ____ amples show how sex-specific selection on behavior Mitochondria also play a central role in apoptosis, 1 ____ 34667_u01_UNCORR_PRF.3d_5_08-27-07 WHY ARE THERE TWO SEXES? 5 a form of cell death that contributes to normal de- the centrosome in periventricular cells and are hy- velopment and to diverse pathological states (Schafer pothesized to regulate formation and orientation of & Kornbluth, 2006; Garrido et al., 2006). It is espe- the mitotic spindle. Proliferation of neural progenitors cially interesting that vertebrates evolved the capacity occurs when spindle fibers run parallel to the ven- for a novel class of molecules (i.e., estrogens and an- tricular epithelium. In contrast, neurogenesis gener- drogens) to influence mitochondia-dependent apo- ally occurs when spindle fibers are perpendicular to ptosis in the nervous system (Nilsen & Brinton, 2004; the ventricular epithelium. Exactly how orientation of Forger, 2006; Lin et al., 2006). the mitotic spindle relates to commitment to a neu- There are several hypotheses for the origin of the ronal fate is unknown, but it is possible that the post- membrane-bound nucleus (Martin, 2005), but two mitotic location of the centrosome (i.e., cell asymmetry basic categories can be distinguished. The first group and microtubule polarity) is vital, like it is to devel- of hypotheses suggests direct evolution of this unique opment of neuronal polarity (de Anda et al., 2005). structure in the initial forms of life (Woese, 1998), Again, we see how an ancient event in the evolution of while the second posits a symbiotic origin for the nu- eukaryotes has implications for neural development. cleus (Dolan et al., 2002). Whether the nucleus evol- While mitochondria and mitosis are important to ved de novo or from an archaebacterial-eubacterial human health, the adaptations most salient to our symbiont, it is clear that microtubules played a central discussion of sex differences are meiosis and syngamy. role in the evolution of eukaryotes. Microtubules are Three simple molecular changes account for the essential for mitosis and are a key component of the transition from mitosis to meiosis. The first change cytoskeleton. Moreover, the first split within the eukar- was in alignment
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