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Evolutionary neurobiology
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Evolutionary neurobiology Richard C. Francis 'ayr distinguished two The chasm that formerly separated The bird brain has proven a fundamentally different evolutionary biology from the research particularly fertile model system explanatoryagendaswithof physiologists and developmental for studies of the sexual differentiain biology - that of the biologists has been partially bridged in tion of the nervous system. Rephysiologists and developmental recent years. An increasing amount of search on the vocal centers of the biologists, concerned with events research In the neurosclences makes bird brain provides perhaps the and properties that underlie the explicit reference to Issues in evolutionary best example in which the neural development and maintenance of biology. Much of this research Is an substrates of a complex behavior individual organisms, and that of attempt to understand structures and have been characterized. A numthe evolutionary biologists, who are functions of the brain as adaptations to an ber of brain nuclei that are sexually concerned with trans-generational animal's physical and social environment. dimorphic are relevant to song events that shape the properties In addition, however, some of this production and/or acquisition, for of populationsL The mechanistic research at the Interface of evolutionary example, the hyperstriatum venexplanations provided by physibiology and neurobiology provides trale pars caudalis (HVc), robust ologists are often referred to as information on Internal evolutionary nucleus of the archistriatum (RA), 'proximate', whereas the typically factors and the way they may constrain magnocellular nucleus of the (though by no means exclusively) evolution by natural selection. anterior neostriatum (MAN) and functionalist explanations offered area Xn,~a (see Fig. 1). Generally, by evolutionary biologists are often these nuclei are larger in males Richard Francis is at the Dept of Psychology, referred to as 'ultimate' (but see than in females. However, species University of California, Berkeley, CA 94720, USA. Ref. 2). The distinction between vary appreciably in the degree to Mayr's two biologies has become which sound production is dimorincreasingly blurred as much phic, and these differences appear recent research is being conducted at their interface3,4. to be related to the mating system. In highly polygynous In part, this has resulted from a critique of selectionist species, females sing little, if at all, whereas in some monogaor functionalist explanations of evolutionary phenmous species, female singing is pronounced. Generally, in omena, which has generated a renewed interest in the comparisons across species, as sex differences in song beway physiological and developmental properties of organ- havior diminish so do the dimorphisms in the song nucleP 3. isms constrain and direct subsequent evolution5; and, in In the monogamous bay wren (Thryothoms nigricapillus), a part, it reflects the desire of some physiologists and de- so-called 'duetting' species in which male and female both velopmental biologists to find an evolutionary context, in sing in a coordinated fashion, the number of testosterone addition to the traditional biomedical framework, for target cells in one song nucleus, the HVc,differs little between their research. Here, I review recent research at the inter- the sexes 14. In the polygynous zebra finch (Taeniopygia face ofevolutionary biology and neurobiology, focusing guttata), however, in which females do not sing, males have on evolutionary neurobiological research concerned significantly more of these cells than the females 13. Morewith reproductive, function and sexual development in over, zebra finch females also lack a well-defined area X. vertebrates. Other parts of the brain are also sexually differentiated and in a way that can best be understood by reference to the From evolutionary biology to neurobiology different selective influences experienced by the two sexes. Neurobiological research has been influenced by evo- The hippocampus has become an increasing focus of attenlutionary biology in several ways. First, there is a long tra- tion for both neurobiologists and behavioral ecologists ~5J6. dition of comparative neuroanatomy in which the goal is to This structure plays an important role in spatial learning understand the evolution of the brain and questions of hom- and memory consolidation. Birds and mammals that cache ology6-9. Recent studies have also probed the phylogeny of food for future consumption16,~7,or that have experienced neuroactive peptides and the genes that encode them ]0, artificial selection for spatial memory, such as the homing relying on information and analytical techniques derived pigeon TM,have larger hippocampi and/or more hippocampal from systematics. Second, interest is growing among neuroneurons than closely related species that do not exhibit this biologists in linking their research to questions concerning behavior. how the organism functions in its environment. There are also sex differences in hippocampal size and activity19,20 (Fig. 2). Comparative studies on voles of the Sexual selection and the brain genus Microtus suggest a role for sexual selection in shaping A basic component of the reproductive process is locating hippocampal sexual dimorphism. In polygynous species, and attracting a mate. Because of fundamental asymmetries such as the meadow vole (M. pennsylvanicus), males have in parental investmentu, males of most species pursue fe- larger home ranges and are more successful in complex males rather than the reverse. Hence, males of many species maze-learning tasks than females. On the other hand, pine have evolved elaborate displays to advertise themselves, for voles (M. pinetorum), which are monogamous and inhabit which there is no correlate among females. Not surprisingly, smaller home ranges, exhibit no dimorphism in spatial bethis behavioral dimorphism is associated with differences havior. The hippocampi of male meadow voles are correin the brain. spondingly larger than those of male pine voles, and the
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REVIEWS Intrasexual dimorphisms in the brain In addition to CNS sexual dimorphisms related to sexual selection, many vertebrates exhibit intrasexual dimorphisms typically among males - associated with alternative reproductive tactics. These male morphs are especially common among teleost fishes. In one such species, the midshipman (Porichthys notatus), the neural correlates of this intrasexual dimorphism are particularly well-characterized 27. This species has two male morphs. Type I males, which comprise about 90% of the male population, defend a breeding territory and display a distinctive vocal behavior to attract females. Type II males are much smaller, generally resemble females and do not vocalize. Rather, these 'satellite' males occupy the periphery of the Type I males' territories and attempt to 'sneak' fertilizations with females attracted to the Type I males. The parts of the nervous system controlling vocalization exhibit a number of intra- and intersexual dimorphisms, with the Type II males resembling females in all respects 28,29. Interestingly, there are also corresponding differences in the development of neurons containing gonadotropinreleasing hormone (GnRH). GnRH neurons are more numerous in the preoptic area (POA) of Type I males than Type 1I males and females 30. The POA and adjacent ventral hypothalamus are the areas of the brain most directly involved in regulating gonadal function and reproductive behavior. GnRH, a key element in the regulation of vertebrate maturation and reproduction, is expressed primarily in this region and the terminal nerve of the ventral telencephalon, as well as in a small region of the mesencephalon (Fig. 3). The platyfish (Xiphophorus maculatus) is another teleost with alternative male reproductive tactics in which there is an associated difference in GnRH expression3L In this case, the genetics of this polymorphism have been established 32. Some males mature precociously at 12-14 weeks, others much later, as a function of alleles at a single genetic locus, the so-called P-locus. This appears to be a balanced polymorphism, because once the male has matured it stops growing. Early-maturing males have a head start at breeding, while later-maturing males seem to accrue an advantage in competition with early-maturing males as a result of their size-advantage. There are corresponding differences in the ontogeny of GnRH expression in three separate neuronal -
Rg. 1. Mid-sagittalview of the passerine brain, showingmajor song control nucleiand their connections.Shadedareasaccumulatetestosterone or its metabolites. HVc, hyperstriatumventrale, pars caudalis; RA, robust nucleusof the archistriatum; MAN,magnocellularnucleus of the anteriorneostriatum;X, area X. The syrinxis the organ of sound production in birds. Adapted, with permission, from Ref. 13.
sexual dimorphism in hippocampus size is greater in meadow voles than in pine voles2L In addition to the variation in hippocampal dimorphism with mating system, two areas of the medial preoptic area-anterior hypothalamus, (MPOA-AH), the anteroventral-periventricular nucleus (AVPV) and the sexually dimorphic nucleus of the preoptic area (SDN-POA), which have been implicated in both reproductive and social behavior, have been shown to be more dimorphic in polygynous voles than in monogamous species 22. Kangaroo rats of the genus Dipodomys exhibit similarities to voles with respect to the relationships between mating systems, foraging habits and hippocampal size 23.The brownheaded cowbird (Molothrus ater), on the other hand, is noteworthy in that the females have larger hippocampi than the males 24. Female cowbirds lay their eggs in the nest of other species, a task for which males provide no assistance. A given female may parasitize several nests in an area. It has been speculated that the sexual dimorphism that exists in this species reflects more selection for spatial learning in females than in males, given their brood parasitic habits. Much more work needs to be done, however, in both birds and mammals to establish the generality of the correlation between hippocampal dimorphism and mating systems. There are other differences in the central nervous systems of monogamous and polygynous voles that are not sexually dimorphic but which may be related to their different mating systems. Oxytocin is a neuropeptide that evolved after the mammalian clade diverged from other vertebrates. This neuropeptide, which is widely distributed in the brain, has been implicated in affiliative behavior and social bonding. In two monogamous species, the prairie vole (M. ochrogaster) and the pine vole (M. pinetorum), specific binding to oxytocin receptors was highest in the prelimbic cortex, nucleus accumbens and the lateral amygdala, among other regions. However, in two polygynous species, the montane vole (M. montanus) and the meadow vole (M. pennsylvanicus), binding was confined to the lateral septum, ventromedial nucleus of the hypothalamus and the cortical nucleus of the amygdala2~. Differences in the distribution of vasopressin, which has been implicated in paternal behavior and alfiliative behavior, have also been demonstrated between monogamous and polygynousvoles26.Much research remains to be done to establish the functional significance of the variation in the distribution of these two peptides. T R E E voL 10, no. 7 J u l y 1995
Right cerebral hemisphere Corpus callosum ~
~
Cerebellum
Ventral hippocampal commissure Rg. 2. Schematicof a rodent(rat) brain showinglocationof hippocampus.Lateral portionsof the forebrainhavebeenremoved.Adapted, with permission, from Ref. 55.
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REVIEWS populations31.The differences in the male maturation morphs may result from the action of alleles at the P locus on these GnRH neurons. Another species complex within this genus exhibits similar male polymorphisms 33, and should provide a fruitful system for evolutionary neurobiologists. Many teleost fishes are sequential hermaphrodites. In most species, individuals mature first as females and subsequently become males (protogyny). In a few species, the reverse occurs (protandry). While both types of sex changers should provide rewarding material for evolutionary neurobiologists interested in the sexual differentiation of the brain, some protogynous :species offer, in addition, the opportunity to examine intrasexual differences associated with alternative male reproductive tactics. These 'diandric' species exhibit two male morphs: 'primary' males that mature first as males, though at a small size, and 'terminal phase' males that have undergone sex change. Again, the two male types exhibit markedly different reproductive behavior, with the terminal phase males controlling territories and the primary males sneak-spawning 34. To date, little neurobiological work has been done on any sex-changing species, but in one diandric species, the bluehead wrasse (Thalassoma bifasciatum), terminal phase males have more GnRH neurons in the POA than do either primary males or females when these estimates are adjusted for body size 3s. Interestingly, in many of these cases of alternate male reproductive morphs, a suite of traits that is female-typical characterizes the less common morph. Further research is needed to establish the developmental mechanism underlying these alternative male developmental trajectories. The Mrican cichlid, Haplochromis burtoni, also has two types of males, though they do not represent distinct morphs. This is, rather, a case where relatively few males occupy a suitable territory (T males) and breed at any given time, whereas the rest (nonterritorial or NT males) are relegated to a nonbreeding status. The NT males are simply 'making the best of a bad job', in essence, biding their time until they can defend a territory themselves. In this sense, they resemble subdominant elephant seals or gorillas. This behavioral flexibility has an interesting neurobiological.correlate. Unlike Xiphophorus and Porichthys, in which the size and number of GnRH neurons in the POA is stable in adults, in Haplochromis the corresponding neurons exhibit remarkable plasticity36 (Fig. 4). This plasticity is confined to the POA population, which projects to the pituitary; it is not exhibited by the terminal nerve or mesencephalic GnRI-I neuron populations. The T males are both more colorful and have larger testes than the NT males. Moreover, T males aggressively dominate NT male.,;of the same size. T males, however, exert much energy in defending their territory and courting females and, in addition, are more vulnerable to predation than the NT males because of their more conspicuous color and behavior. As a result, the tenure of T males is relatively short, and any vacancy is quickly filled by an NT male, which almost immediately adopts the coloration and behavior of a T male. These external changes are accompanied by a dramatic increase in size of testes and in the soma size of GnRI-I neurons in the POA of these males. Conversely, males making the reverse transition (from T to NT) show a reduction in testes weight and in the size of POA GnRH neurons. This plasticity in the GnRH neurons allows the NT males to upregulate the entire hypothalamic-pituitary-gonadal (HPG) axis when conditions permit. Presumably, the reverse transition, which is equally dramatic, results in a reduction in energy expenditure for reproductive function in males for 278
Optic
Fig. 3. Mid-sagittal view of a typical teleost brain (Haplochromis burtoni). POA,preoptic area; TN, terminal nerve; MES, mesencephalon. Asterisks indicate GnRH immunoreactive neurons.
whom there is no prospect for successful mating. This surprising neural plasticity in Haplochromis GnRH neurons provides insight into a mechanism for the phenomenon, widespread among vertebrates, of the social regulation of maturation and adult reproduction.
From neurobiology to evolutionary biology In addition to the functionalist studies described above, a significant amount of evolutionary neurobiological research has been concerned with how certain details of the nervous system are relevant to some longstanding issues in evolutionary biology. The impetus here has been the reemphasis on internal factors in evolution resulting from the critique of selectionism. In essence, this amounts to a characterization of how the developmental systems of ancestral species influence and constrain the phenotypes of their descendants, independently of, and sometimes in opposition to, the effects of selection. Most of this research has been concerned with gross morphology, particularly limb development. Recently, however, attention has also been directed towards the nervous system. Ryan's 'sensory exploitation' hypothesis37of sexual selection is an example of an internalist approach to an evolutionary issue in which neurobiological knowledge will ultimately figure prominently. In this it stands in marked contrast to the 'good genes' and Fisherian runaway selection hypotheses, which make no reference to constraints imposed by existing physiological and anatomical states of the organism.
A structuralist approach to brain evolution Recent comparative research among amphibians 38provides a paradigmatic example of how neurobiology might prove informative with respect to the internal dimension of evolution. This research demonstrated an inverse correlation betweencomplexity of the optic tectum, as measured by the number of cell types, and mean cell (soma) size. Moreover, this complexity was not associated with variation in the functional demands on this important component of the visual system. For example, in the bollitoglossine salamanders, stereoscopic vision is highly developed, yet the optic tecta are among the simplest, and mean cell soma size is among the largest. Rather, the driving force in determining the complexity of this brain region appears to be genome size, which itself does not vary systematically with ecological conditions. Genome size itself seems to vary according to the dynamics of intragenomic competition and the resulting differences in the amount of selfish DNA. As genome size increases, the mean cell size within the tecta also increases, TREE vol. 10, no. 7 J u l y 1995
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Non-territorial
Territorial
Fig. 4. Representative preoptic area GnRH neurons of non-territorial and territorial males, labelled with antibody to salmon GnRH. Scale bar= 50 i~m.
and complexity decreases. Hence, some salamander taxa, which possess the largest genomes among vertebrates, have the simplest optic tecta despite their visual specializations. The authors refer to their account as a structuralist or hierarchical explanation, in contrast to the prevailing current of functionalism, in which the comparative method is used primarily to warrant adaptationist claims. This sort of approach will be worth pursuing, for example, in the hippocampus research described above.
The brain and parthenogenesis
courtship behavior and/or sperm of other closely related species 41. In the all-female lizard, C. uniparens, this stimulation is achieved through pseudomale behavior42 in which one female adopts the characteristic male mating posture during the iuteal phase of the ovarian cycle, and the female mating posture during the follicular phase (Fig. 5). The ventral medial hypothalamus (VMH), which contains both estradiol and progesterone receptors, is involved in the regulation of female receptive behavior in all vertebrates, and C. uniparens is no exception. In the bisexual congener, C. inornatus, male mating behavior is androgen dependent and regulated in the anterior POA. In contrast, in the allfemale C. uniparens, the luteal hormone progesterone has been coopted as the neuroendocrine signal stimulating male-like behavior. This is but one example of a neuroendocrine compensation that occurred in order for C. uniparens to survive as a unisexual species (see Ref. 9 for another example concerning estradiol receptor regulation in the
An issue that has long engaged evolutionary biologists concerns the evolution and maintenance of sexual reproduction39,4°.Asexuality is extremely rare among vertebrates relative to many other taxa. According to Williams40,this resuits from a constraint of some kind, and virtually all sexual reproduction among vertebrates is maladaptive. He claims that when exclusively sexual reproduction has evolved within a lineage, it is difficult to evolve parthenogenesis. As one obstacle, Williams cites the difficulty of altering meiosis. In addition, among vertebrates, prolonged selection Behavior shaping the sexual differentiation process may be diffiFemale-like Male-like Female-like Male-like cult to reverse. Some recent research on a parthenogenic lizard, Cnemidophorus uniparens, may shed some light on this. Ovary The rare examples of parthenogenic reproduction among vertebrates that do Oviduct exist indicate that one of the biggest hurdles to surmount is devising a means to stimelate the oocyte to mature and implant without the stimulaHormones tion provided by male courtship and mating. Whether they reproduce sexually or Fig. 5. Relations between male- and female-like pseudosexual behavior in Cnemidophorusuniparens and circulating levasexually, vertebrates need to els of gonadal steroids during different stages of the reproductive cycle. Ovarian state is denoted by circles. Adapted, with mate. Among some parthenopermission, from Ref. 3. genic teleosts, this is achieved through 'parasitizing' the T R E E v o l . 10, n o .
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REVIEWS hypothalamus). Interestingly, these functional differences between the unisexual and bisexual species are not accompanied by any obvious structural differences in the relevant brain areas. Rather, the brains of the all-female C. uniparens and of female C. inornatus are indistinguishable. Further understanding of the neuroendocrine adaptations in Cnemidophorus will not only illuminate how asexual reproduction can be achieved in a vertebrate, but also, perhaps, why it is not more common•
The brain and sex cl~ange In sexually reproducing multicellular organisms, sexual differentiation is an important component of development. Among vertebrates;, the degree to which this process is canalized varies widely, and has an obvious taxonomic component 43,44. Birds and mammals exhibit highly canalized sexual differentiation, amphibians and reptiles are more plastic, and teleost fishes are extremely labile, though they all share essentially the same reproductive system (hypothalamic-pituitary.-gonadal axis). Some examples of this lability include determination of primary sex by social 45,46and physical environmental factors47; hormonal manipulations of sex and sex change4S; bisexuality within clones 49and prematurational sex change46,~°.The most prominent expression of this lability is post-maturational sex change, which is common in teleosts but virtually absent in tetrapods 43,44. Ghiselin's size-advantage model51, which is based on considerations of sex differences in size/fitness trajectories, nicely predicts the conditions under which sex change will occur, its timing, and the form it will take (protogyny or protandry). But according to this model, many tetrapods should change sex as well. The fact that they do not suggests that sex change in teleosts is not solely the result of something distinctive about their selective milieu relative to • r other vertebrate taxa, but that sexual development in tetrapods is constrained in some way that teleost sexual development is not. That is, perhaps elephant seals or sage grouse, both species in which variance for male reproductive success is very high, would change sex if it were possible. One way in which teleost sexual development may differ from that of most other vertebrates is in the primacy of the brain in sexual development. In teleosts, there is evidence that sex differentiation is initiated in the brain and that brain sex determines gonadal sex 44. This would account for the fact that sexual differentiation in teleosts is so susceptible to influence by social and other environmental cues. The search is under way for neuronal populations in the hypothalamus or ventral telencephalon, where this process may be initiated. Experiiments demonstrating the efficacy of both gonadotropins 52and GnRHs3 in inducing sex change suggest that wherever the process is initiated, GnRH neurons that project to the pituitary constitute the final common pathway for the CNS influence on the gonads. Alternatively, brain sex may be communicated to the gonad through direct neural connections s4, or both through these direct connections and through the pituitary. It is important to establish whether this aspect of teleost sexual development, along with its generally protogynous pattern, is the primitive condition in vertebrates. If so, given the obvious advantages of this lability, the focus should be on why it has been progressively lost in tetrapods through a canalization of gonadal development, such that sex differentiation is initiated in the gonads themselves. Much of the explanation for the prevalence of sex change among teleosts may be accounted for by this general sexual lability, which, in turn, results from the primacy of the brain in their sexual differentiation. The size-advantage model explains why and
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when a species with this sort of lability ch~ges sex; it does not, however, explain why sex change is largely restricted to teleosts.
Conclusions The emerging field of evolutionary neurobiology is still in its infancy. Research conducted to date indicates that both neurobiologists and evolutionary biologists have much to gain from their increased interactions. The research reviewed here suggests that evolutionary neurobiology will benefit if both externalist (natural selection) and internalist (developmental and physiological constraints) evolutionary perspectives are seriously entertained. Moreover, if Mayr's two explanatory agendas are to find some fruitful interaction here, the temptation to subsume one within the other must be resisted.
Acknowledgements I thank George Barlow, Michael Bell, Tamara Bushnik, David Crews, John Godwin, Lucille Jacobs, George Losey, David Wake and Irving Zucker for their helpful comments.
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REVIEWS 31 Halpern-Seboldt.L.R.,Schreibman, M.P. and Margolis-Nunno, H. (1986) J. Exp. Zool. 240, 245-257 32 Kallman, K.D., Schreibman, M.P. and Borkoski, V. (1973) Gen. Comp. Endocrin. 21,287-304 33 Kallman, K.D. (1983) Copeia 1983, 755-769 34 Roede, M.J. (1990) Bijdr. Dierkd. 60, 225-232 35 Grober, M.S. and Bass, A.H. (1991) Brain Behav. Evol. 38, 302-312 36 Francis, R.C., Soma, K. and Fernald, R.D. (1993)Proc. NatlAcad. Sci. USA 90, 7794-7798 37 Ryan,M.J. and Keddy-Hector, A. (1992) Am. Nat. 139, $4-$35 38 Roth, G., Blanke, J. and Wake, D.B. (1994) Proc. NatlAcad. Sci. USA 91, 4796-4800 39 Michod, R.E. and Levin, B.R., eds (1988) The Evolution of Sex, Sinauer 40 Williams,G.C. (1975) Sex and Evolution, Princeton University Press 41 Schultz, R.J. (1979)Evol. Biol. 10, 277-331 42 Crews, D. and Young, L.J. (1991) Anim. Behav. 42, 512-514 43 Policansky, D. (1982)Annu. Rev. Ecol. Syst. 13, 471-495
44 Francis, R.C. (1992) Q. Rev. Biol. 67, 1-18 45 Francis, R.C. and Barlow, G.W. (1993)Proc. Natl Acad. ScL USA 90, 10673-10675 46 Francis, R.C. (1984)BehaviourgO, 25-45 47 Conover, D.O. and Heins, 8.W. (1987) Nature, 326, 496-498 48 Hunter, G.A. and Donaldson, E.M. (1983) in Fish Physiology (Vol. 9B) (Hoar, W.S., Randall, D.J. and Donaldson, E.M., eds), pp. 222-303, Academic Press 49 Streisinger, G., Walker, C., Dower, N., Knauber, D. and Singer, F. (1981) Nqture 291,293-296 50 Takahashi, H. and Shimizn, M. (1983)Bull. Fac. Fish. Hokkaido Univ. 34, 69-78 51 Ghiselin, M.T. (1969) Q. Rev. Biol. 44, 189-208 52 Koulish, S. and Kramer, C.R. (1989)J. Exp. Zool. 252, 156-168 53 Kramer, C.R., Caddell, M.T. and Bubenheimer-Livolsi, L. (1993) J. Fish. Biol. 42, 185-195 54 Crews,D. (1993) Brain Behav. Evol. 42, 202-214 55 O'Keefe, J. and Nadel, L. (1978) The Hippocampus as a Cognitive Map, Oxford University Press
Sex determination and population biology in the Hymenoptera James M. Cook and Ross H. Crozier ' ale haploidy is a distincThe Hymenoptera (ants, bees, wasps and sex determination load equals 1/k tive characteristic of the sawflles) display a great variety of social (Box 1) but it increases dramatiHymenoptera and has systems and sex ratios and have played a cally with inbreeding (Box 2). It is , important consequences key role in the development and testing of important to distinguish between for sex allocation and social evomany evolutionary models. Traditionally, the proportion of diploids that are lution. However, it has been known considerable emphasis was placed on the male (i.e. sex determination load) 4 for over 50 years ~that, owing to a fact that hymenopterans have haploid and the proportion of males that system of complementary sex demales and diploid females but It is now are diploid5,6.Both depend on allelic termination (CSD), sterile, diploid clear that many species also regularly diversity and mating structure but males are also produced in some produce sterile, diploid males. Recent the latter depends also on the proHymenoptera. Developments in studies explore the diverse ways in which portion of eggs fertilized, which population biology have largely production of these diploid males varies considerably within and beignored CSD, which, as recently as influences selection on mating systems, tween hymenopteran species. In 1977 (Ref. 2), had been demonsex ratios and social behaviour. this article, quantitative uses of strated clearly in only two genera. the term diploid male production However, subsequent studies show (DMP) refer to the sex determinaJames Cook is at the Dept of Biology and NERC that CSD occurs in many disparate tion load. Centre for Population Biology, Imperial College, species of Hymenoptera. (Diploid While the sterility of diploid Silwood Park, Ascot, UK SL5 7PY; Ross Crozier is males have now been reported in males is a general phenomenon at the School of Genetics and Human Variation, over 30 species3.) It is no longer La Trobe University, Bundoora 3083, Victoria, Australia. (Box 2), other aspects of their bireasonable to ignore the effects of ology are more variable. They reCSD on population biology and it semble haploid males very closely has been considered explicitly in several recent studies, in Bracon 1 but are clearly larger ranging from the evolution of signalling to the rearing of para- than haploid males in some other species 7-10. In sawflies, sitoids for biological control. This new synthesis of genetics this large size difference makes it difficult for diploid males and population biology promises to add considerably to our to copulate successfully TMbut this is probably not the case understanding of hymenopteran biology. in most other species. Finally, although Bracon hebetor diploid males have very high larval mortality rates 1, diploid Complementary sex determination and diploid males males of most species appear to have fairly normal viability. Single-locus CSD, which depends on multiple alleles at a The taxonomic distribution of single-locus CSD is poorly single locus (Box 1), was first described in the parasitoid understood (Box 3), but species with single-locus CSD range wasp Bracon hebetoP. Heterozygotes (AiAj) are female while from non-social parasitoid wasps and sawflies to eusocial homozygotes (A.r4i or A.r4j) and hemizygotes (Ai or Aj) are bees and ants. Thus, at least some representatives of each diploid and haploid males, respectivelyL Diploid males pro- of the main hymenopteran lifestyles are subject to the probduce diploid sperm and are effectively sterile (Box 2), im- lem of DMP. It is also clear that there is a strong negative posing a genetic load on the population. In a random-mating correlation between the occurrence of inbreeding and CSD, population with k equally common sex alleles, this genetic presumably because inbreeding increases DMP (Box 2).
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Evolutionary neurobiology Richard C. Francis 'ayr distinguished two The chasm that formerly separated The bird brain has proven a fundamentally different evolutionary biology from the research particularly fertile model system explanatoryagendaswithof physiologists and developmental for studies of the sexual differentiain biology - that of the biologists has been partially bridged in tion of the nervous system. Rephysiologists and developmental recent years. An increasing amount of search on the vocal centers of the biologists, concerned with events research In the neurosclences makes bird brain provides perhaps the and properties that underlie the explicit reference to Issues in evolutionary best example in which the neural development and maintenance of biology. Much of this research Is an substrates of a complex behavior individual organisms, and that of attempt to understand structures and have been characterized. A numthe evolutionary biologists, who are functions of the brain as adaptations to an ber of brain nuclei that are sexually concerned with trans-generational animal's physical and social environment. dimorphic are relevant to song events that shape the properties In addition, however, some of this production and/or acquisition, for of populationsL The mechanistic research at the Interface of evolutionary example, the hyperstriatum venexplanations provided by physibiology and neurobiology provides trale pars caudalis (HVc), robust ologists are often referred to as information on Internal evolutionary nucleus of the archistriatum (RA), 'proximate', whereas the typically factors and the way they may constrain magnocellular nucleus of the (though by no means exclusively) evolution by natural selection. anterior neostriatum (MAN) and functionalist explanations offered area Xn,~a (see Fig. 1). Generally, by evolutionary biologists are often these nuclei are larger in males Richard Francis is at the Dept of Psychology, referred to as 'ultimate' (but see than in females. However, species University of California, Berkeley, CA 94720, USA. Ref. 2). The distinction between vary appreciably in the degree to Mayr's two biologies has become which sound production is dimorincreasingly blurred as much phic, and these differences appear recent research is being conducted at their interface3,4. to be related to the mating system. In highly polygynous In part, this has resulted from a critique of selectionist species, females sing little, if at all, whereas in some monogaor functionalist explanations of evolutionary phenmous species, female singing is pronounced. Generally, in omena, which has generated a renewed interest in the comparisons across species, as sex differences in song beway physiological and developmental properties of organ- havior diminish so do the dimorphisms in the song nucleP 3. isms constrain and direct subsequent evolution5; and, in In the monogamous bay wren (Thryothoms nigricapillus), a part, it reflects the desire of some physiologists and de- so-called 'duetting' species in which male and female both velopmental biologists to find an evolutionary context, in sing in a coordinated fashion, the number of testosterone addition to the traditional biomedical framework, for target cells in one song nucleus, the HVc,differs little between their research. Here, I review recent research at the inter- the sexes 14. In the polygynous zebra finch (Taeniopygia face ofevolutionary biology and neurobiology, focusing guttata), however, in which females do not sing, males have on evolutionary neurobiological research concerned significantly more of these cells than the females 13. Morewith reproductive, function and sexual development in over, zebra finch females also lack a well-defined area X. vertebrates. Other parts of the brain are also sexually differentiated and in a way that can best be understood by reference to the From evolutionary biology to neurobiology different selective influences experienced by the two sexes. Neurobiological research has been influenced by evo- The hippocampus has become an increasing focus of attenlutionary biology in several ways. First, there is a long tra- tion for both neurobiologists and behavioral ecologists ~5J6. dition of comparative neuroanatomy in which the goal is to This structure plays an important role in spatial learning understand the evolution of the brain and questions of hom- and memory consolidation. Birds and mammals that cache ology6-9. Recent studies have also probed the phylogeny of food for future consumption16,~7,or that have experienced neuroactive peptides and the genes that encode them ]0, artificial selection for spatial memory, such as the homing relying on information and analytical techniques derived pigeon TM,have larger hippocampi and/or more hippocampal from systematics. Second, interest is growing among neuroneurons than closely related species that do not exhibit this biologists in linking their research to questions concerning behavior. how the organism functions in its environment. There are also sex differences in hippocampal size and activity19,20 (Fig. 2). Comparative studies on voles of the Sexual selection and the brain genus Microtus suggest a role for sexual selection in shaping A basic component of the reproductive process is locating hippocampal sexual dimorphism. In polygynous species, and attracting a mate. Because of fundamental asymmetries such as the meadow vole (M. pennsylvanicus), males have in parental investmentu, males of most species pursue fe- larger home ranges and are more successful in complex males rather than the reverse. Hence, males of many species maze-learning tasks than females. On the other hand, pine have evolved elaborate displays to advertise themselves, for voles (M. pinetorum), which are monogamous and inhabit which there is no correlate among females. Not surprisingly, smaller home ranges, exhibit no dimorphism in spatial bethis behavioral dimorphism is associated with differences havior. The hippocampi of male meadow voles are correin the brain. spondingly larger than those of male pine voles, and the
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REVIEWS Intrasexual dimorphisms in the brain In addition to CNS sexual dimorphisms related to sexual selection, many vertebrates exhibit intrasexual dimorphisms typically among males - associated with alternative reproductive tactics. These male morphs are especially common among teleost fishes. In one such species, the midshipman (Porichthys notatus), the neural correlates of this intrasexual dimorphism are particularly well-characterized 27. This species has two male morphs. Type I males, which comprise about 90% of the male population, defend a breeding territory and display a distinctive vocal behavior to attract females. Type II males are much smaller, generally resemble females and do not vocalize. Rather, these 'satellite' males occupy the periphery of the Type I males' territories and attempt to 'sneak' fertilizations with females attracted to the Type I males. The parts of the nervous system controlling vocalization exhibit a number of intra- and intersexual dimorphisms, with the Type II males resembling females in all respects 28,29. Interestingly, there are also corresponding differences in the development of neurons containing gonadotropinreleasing hormone (GnRH). GnRH neurons are more numerous in the preoptic area (POA) of Type I males than Type 1I males and females 30. The POA and adjacent ventral hypothalamus are the areas of the brain most directly involved in regulating gonadal function and reproductive behavior. GnRH, a key element in the regulation of vertebrate maturation and reproduction, is expressed primarily in this region and the terminal nerve of the ventral telencephalon, as well as in a small region of the mesencephalon (Fig. 3). The platyfish (Xiphophorus maculatus) is another teleost with alternative male reproductive tactics in which there is an associated difference in GnRH expression3L In this case, the genetics of this polymorphism have been established 32. Some males mature precociously at 12-14 weeks, others much later, as a function of alleles at a single genetic locus, the so-called P-locus. This appears to be a balanced polymorphism, because once the male has matured it stops growing. Early-maturing males have a head start at breeding, while later-maturing males seem to accrue an advantage in competition with early-maturing males as a result of their size-advantage. There are corresponding differences in the ontogeny of GnRH expression in three separate neuronal -
Rg. 1. Mid-sagittalview of the passerine brain, showingmajor song control nucleiand their connections.Shadedareasaccumulatetestosterone or its metabolites. HVc, hyperstriatumventrale, pars caudalis; RA, robust nucleusof the archistriatum; MAN,magnocellularnucleus of the anteriorneostriatum;X, area X. The syrinxis the organ of sound production in birds. Adapted, with permission, from Ref. 13.
sexual dimorphism in hippocampus size is greater in meadow voles than in pine voles2L In addition to the variation in hippocampal dimorphism with mating system, two areas of the medial preoptic area-anterior hypothalamus, (MPOA-AH), the anteroventral-periventricular nucleus (AVPV) and the sexually dimorphic nucleus of the preoptic area (SDN-POA), which have been implicated in both reproductive and social behavior, have been shown to be more dimorphic in polygynous voles than in monogamous species 22. Kangaroo rats of the genus Dipodomys exhibit similarities to voles with respect to the relationships between mating systems, foraging habits and hippocampal size 23.The brownheaded cowbird (Molothrus ater), on the other hand, is noteworthy in that the females have larger hippocampi than the males 24. Female cowbirds lay their eggs in the nest of other species, a task for which males provide no assistance. A given female may parasitize several nests in an area. It has been speculated that the sexual dimorphism that exists in this species reflects more selection for spatial learning in females than in males, given their brood parasitic habits. Much more work needs to be done, however, in both birds and mammals to establish the generality of the correlation between hippocampal dimorphism and mating systems. There are other differences in the central nervous systems of monogamous and polygynous voles that are not sexually dimorphic but which may be related to their different mating systems. Oxytocin is a neuropeptide that evolved after the mammalian clade diverged from other vertebrates. This neuropeptide, which is widely distributed in the brain, has been implicated in affiliative behavior and social bonding. In two monogamous species, the prairie vole (M. ochrogaster) and the pine vole (M. pinetorum), specific binding to oxytocin receptors was highest in the prelimbic cortex, nucleus accumbens and the lateral amygdala, among other regions. However, in two polygynous species, the montane vole (M. montanus) and the meadow vole (M. pennsylvanicus), binding was confined to the lateral septum, ventromedial nucleus of the hypothalamus and the cortical nucleus of the amygdala2~. Differences in the distribution of vasopressin, which has been implicated in paternal behavior and alfiliative behavior, have also been demonstrated between monogamous and polygynousvoles26.Much research remains to be done to establish the functional significance of the variation in the distribution of these two peptides. T R E E voL 10, no. 7 J u l y 1995
Right cerebral hemisphere Corpus callosum ~
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Ventral hippocampal commissure Rg. 2. Schematicof a rodent(rat) brain showinglocationof hippocampus.Lateral portionsof the forebrainhavebeenremoved.Adapted, with permission, from Ref. 55.
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REVIEWS populations31.The differences in the male maturation morphs may result from the action of alleles at the P locus on these GnRH neurons. Another species complex within this genus exhibits similar male polymorphisms 33, and should provide a fruitful system for evolutionary neurobiologists. Many teleost fishes are sequential hermaphrodites. In most species, individuals mature first as females and subsequently become males (protogyny). In a few species, the reverse occurs (protandry). While both types of sex changers should provide rewarding material for evolutionary neurobiologists interested in the sexual differentiation of the brain, some protogynous :species offer, in addition, the opportunity to examine intrasexual differences associated with alternative male reproductive tactics. These 'diandric' species exhibit two male morphs: 'primary' males that mature first as males, though at a small size, and 'terminal phase' males that have undergone sex change. Again, the two male types exhibit markedly different reproductive behavior, with the terminal phase males controlling territories and the primary males sneak-spawning 34. To date, little neurobiological work has been done on any sex-changing species, but in one diandric species, the bluehead wrasse (Thalassoma bifasciatum), terminal phase males have more GnRH neurons in the POA than do either primary males or females when these estimates are adjusted for body size 3s. Interestingly, in many of these cases of alternate male reproductive morphs, a suite of traits that is female-typical characterizes the less common morph. Further research is needed to establish the developmental mechanism underlying these alternative male developmental trajectories. The Mrican cichlid, Haplochromis burtoni, also has two types of males, though they do not represent distinct morphs. This is, rather, a case where relatively few males occupy a suitable territory (T males) and breed at any given time, whereas the rest (nonterritorial or NT males) are relegated to a nonbreeding status. The NT males are simply 'making the best of a bad job', in essence, biding their time until they can defend a territory themselves. In this sense, they resemble subdominant elephant seals or gorillas. This behavioral flexibility has an interesting neurobiological.correlate. Unlike Xiphophorus and Porichthys, in which the size and number of GnRH neurons in the POA is stable in adults, in Haplochromis the corresponding neurons exhibit remarkable plasticity36 (Fig. 4). This plasticity is confined to the POA population, which projects to the pituitary; it is not exhibited by the terminal nerve or mesencephalic GnRI-I neuron populations. The T males are both more colorful and have larger testes than the NT males. Moreover, T males aggressively dominate NT male.,;of the same size. T males, however, exert much energy in defending their territory and courting females and, in addition, are more vulnerable to predation than the NT males because of their more conspicuous color and behavior. As a result, the tenure of T males is relatively short, and any vacancy is quickly filled by an NT male, which almost immediately adopts the coloration and behavior of a T male. These external changes are accompanied by a dramatic increase in size of testes and in the soma size of GnRI-I neurons in the POA of these males. Conversely, males making the reverse transition (from T to NT) show a reduction in testes weight and in the size of POA GnRH neurons. This plasticity in the GnRH neurons allows the NT males to upregulate the entire hypothalamic-pituitary-gonadal (HPG) axis when conditions permit. Presumably, the reverse transition, which is equally dramatic, results in a reduction in energy expenditure for reproductive function in males for 278
Optic
Fig. 3. Mid-sagittal view of a typical teleost brain (Haplochromis burtoni). POA,preoptic area; TN, terminal nerve; MES, mesencephalon. Asterisks indicate GnRH immunoreactive neurons.
whom there is no prospect for successful mating. This surprising neural plasticity in Haplochromis GnRH neurons provides insight into a mechanism for the phenomenon, widespread among vertebrates, of the social regulation of maturation and adult reproduction.
From neurobiology to evolutionary biology In addition to the functionalist studies described above, a significant amount of evolutionary neurobiological research has been concerned with how certain details of the nervous system are relevant to some longstanding issues in evolutionary biology. The impetus here has been the reemphasis on internal factors in evolution resulting from the critique of selectionism. In essence, this amounts to a characterization of how the developmental systems of ancestral species influence and constrain the phenotypes of their descendants, independently of, and sometimes in opposition to, the effects of selection. Most of this research has been concerned with gross morphology, particularly limb development. Recently, however, attention has also been directed towards the nervous system. Ryan's 'sensory exploitation' hypothesis37of sexual selection is an example of an internalist approach to an evolutionary issue in which neurobiological knowledge will ultimately figure prominently. In this it stands in marked contrast to the 'good genes' and Fisherian runaway selection hypotheses, which make no reference to constraints imposed by existing physiological and anatomical states of the organism.
A structuralist approach to brain evolution Recent comparative research among amphibians 38provides a paradigmatic example of how neurobiology might prove informative with respect to the internal dimension of evolution. This research demonstrated an inverse correlation betweencomplexity of the optic tectum, as measured by the number of cell types, and mean cell (soma) size. Moreover, this complexity was not associated with variation in the functional demands on this important component of the visual system. For example, in the bollitoglossine salamanders, stereoscopic vision is highly developed, yet the optic tecta are among the simplest, and mean cell soma size is among the largest. Rather, the driving force in determining the complexity of this brain region appears to be genome size, which itself does not vary systematically with ecological conditions. Genome size itself seems to vary according to the dynamics of intragenomic competition and the resulting differences in the amount of selfish DNA. As genome size increases, the mean cell size within the tecta also increases, TREE vol. 10, no. 7 J u l y 1995
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Fig. 4. Representative preoptic area GnRH neurons of non-territorial and territorial males, labelled with antibody to salmon GnRH. Scale bar= 50 i~m.
and complexity decreases. Hence, some salamander taxa, which possess the largest genomes among vertebrates, have the simplest optic tecta despite their visual specializations. The authors refer to their account as a structuralist or hierarchical explanation, in contrast to the prevailing current of functionalism, in which the comparative method is used primarily to warrant adaptationist claims. This sort of approach will be worth pursuing, for example, in the hippocampus research described above.
The brain and parthenogenesis
courtship behavior and/or sperm of other closely related species 41. In the all-female lizard, C. uniparens, this stimulation is achieved through pseudomale behavior42 in which one female adopts the characteristic male mating posture during the iuteal phase of the ovarian cycle, and the female mating posture during the follicular phase (Fig. 5). The ventral medial hypothalamus (VMH), which contains both estradiol and progesterone receptors, is involved in the regulation of female receptive behavior in all vertebrates, and C. uniparens is no exception. In the bisexual congener, C. inornatus, male mating behavior is androgen dependent and regulated in the anterior POA. In contrast, in the allfemale C. uniparens, the luteal hormone progesterone has been coopted as the neuroendocrine signal stimulating male-like behavior. This is but one example of a neuroendocrine compensation that occurred in order for C. uniparens to survive as a unisexual species (see Ref. 9 for another example concerning estradiol receptor regulation in the
An issue that has long engaged evolutionary biologists concerns the evolution and maintenance of sexual reproduction39,4°.Asexuality is extremely rare among vertebrates relative to many other taxa. According to Williams40,this resuits from a constraint of some kind, and virtually all sexual reproduction among vertebrates is maladaptive. He claims that when exclusively sexual reproduction has evolved within a lineage, it is difficult to evolve parthenogenesis. As one obstacle, Williams cites the difficulty of altering meiosis. In addition, among vertebrates, prolonged selection Behavior shaping the sexual differentiation process may be diffiFemale-like Male-like Female-like Male-like cult to reverse. Some recent research on a parthenogenic lizard, Cnemidophorus uniparens, may shed some light on this. Ovary The rare examples of parthenogenic reproduction among vertebrates that do Oviduct exist indicate that one of the biggest hurdles to surmount is devising a means to stimelate the oocyte to mature and implant without the stimulaHormones tion provided by male courtship and mating. Whether they reproduce sexually or Fig. 5. Relations between male- and female-like pseudosexual behavior in Cnemidophorusuniparens and circulating levasexually, vertebrates need to els of gonadal steroids during different stages of the reproductive cycle. Ovarian state is denoted by circles. Adapted, with mate. Among some parthenopermission, from Ref. 3. genic teleosts, this is achieved through 'parasitizing' the T R E E v o l . 10, n o .
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REVIEWS hypothalamus). Interestingly, these functional differences between the unisexual and bisexual species are not accompanied by any obvious structural differences in the relevant brain areas. Rather, the brains of the all-female C. uniparens and of female C. inornatus are indistinguishable. Further understanding of the neuroendocrine adaptations in Cnemidophorus will not only illuminate how asexual reproduction can be achieved in a vertebrate, but also, perhaps, why it is not more common•
The brain and sex cl~ange In sexually reproducing multicellular organisms, sexual differentiation is an important component of development. Among vertebrates;, the degree to which this process is canalized varies widely, and has an obvious taxonomic component 43,44. Birds and mammals exhibit highly canalized sexual differentiation, amphibians and reptiles are more plastic, and teleost fishes are extremely labile, though they all share essentially the same reproductive system (hypothalamic-pituitary.-gonadal axis). Some examples of this lability include determination of primary sex by social 45,46and physical environmental factors47; hormonal manipulations of sex and sex change4S; bisexuality within clones 49and prematurational sex change46,~°.The most prominent expression of this lability is post-maturational sex change, which is common in teleosts but virtually absent in tetrapods 43,44. Ghiselin's size-advantage model51, which is based on considerations of sex differences in size/fitness trajectories, nicely predicts the conditions under which sex change will occur, its timing, and the form it will take (protogyny or protandry). But according to this model, many tetrapods should change sex as well. The fact that they do not suggests that sex change in teleosts is not solely the result of something distinctive about their selective milieu relative to • r other vertebrate taxa, but that sexual development in tetrapods is constrained in some way that teleost sexual development is not. That is, perhaps elephant seals or sage grouse, both species in which variance for male reproductive success is very high, would change sex if it were possible. One way in which teleost sexual development may differ from that of most other vertebrates is in the primacy of the brain in sexual development. In teleosts, there is evidence that sex differentiation is initiated in the brain and that brain sex determines gonadal sex 44. This would account for the fact that sexual differentiation in teleosts is so susceptible to influence by social and other environmental cues. The search is under way for neuronal populations in the hypothalamus or ventral telencephalon, where this process may be initiated. Experiiments demonstrating the efficacy of both gonadotropins 52and GnRHs3 in inducing sex change suggest that wherever the process is initiated, GnRH neurons that project to the pituitary constitute the final common pathway for the CNS influence on the gonads. Alternatively, brain sex may be communicated to the gonad through direct neural connections s4, or both through these direct connections and through the pituitary. It is important to establish whether this aspect of teleost sexual development, along with its generally protogynous pattern, is the primitive condition in vertebrates. If so, given the obvious advantages of this lability, the focus should be on why it has been progressively lost in tetrapods through a canalization of gonadal development, such that sex differentiation is initiated in the gonads themselves. Much of the explanation for the prevalence of sex change among teleosts may be accounted for by this general sexual lability, which, in turn, results from the primacy of the brain in their sexual differentiation. The size-advantage model explains why and
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when a species with this sort of lability ch~ges sex; it does not, however, explain why sex change is largely restricted to teleosts.
Conclusions The emerging field of evolutionary neurobiology is still in its infancy. Research conducted to date indicates that both neurobiologists and evolutionary biologists have much to gain from their increased interactions. The research reviewed here suggests that evolutionary neurobiology will benefit if both externalist (natural selection) and internalist (developmental and physiological constraints) evolutionary perspectives are seriously entertained. Moreover, if Mayr's two explanatory agendas are to find some fruitful interaction here, the temptation to subsume one within the other must be resisted.
Acknowledgements I thank George Barlow, Michael Bell, Tamara Bushnik, David Crews, John Godwin, Lucille Jacobs, George Losey, David Wake and Irving Zucker for their helpful comments.
References 1 2 3 4 5 6 7 8 9 10 11 12 13
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Sex determination and population biology in the Hymenoptera James M. Cook and Ross H. Crozier ' ale haploidy is a distincThe Hymenoptera (ants, bees, wasps and sex determination load equals 1/k tive characteristic of the sawflles) display a great variety of social (Box 1) but it increases dramatiHymenoptera and has systems and sex ratios and have played a cally with inbreeding (Box 2). It is , important consequences key role in the development and testing of important to distinguish between for sex allocation and social evomany evolutionary models. Traditionally, the proportion of diploids that are lution. However, it has been known considerable emphasis was placed on the male (i.e. sex determination load) 4 for over 50 years ~that, owing to a fact that hymenopterans have haploid and the proportion of males that system of complementary sex demales and diploid females but It is now are diploid5,6.Both depend on allelic termination (CSD), sterile, diploid clear that many species also regularly diversity and mating structure but males are also produced in some produce sterile, diploid males. Recent the latter depends also on the proHymenoptera. Developments in studies explore the diverse ways in which portion of eggs fertilized, which population biology have largely production of these diploid males varies considerably within and beignored CSD, which, as recently as influences selection on mating systems, tween hymenopteran species. In 1977 (Ref. 2), had been demonsex ratios and social behaviour. this article, quantitative uses of strated clearly in only two genera. the term diploid male production However, subsequent studies show (DMP) refer to the sex determinaJames Cook is at the Dept of Biology and NERC that CSD occurs in many disparate tion load. Centre for Population Biology, Imperial College, species of Hymenoptera. (Diploid While the sterility of diploid Silwood Park, Ascot, UK SL5 7PY; Ross Crozier is males have now been reported in males is a general phenomenon at the School of Genetics and Human Variation, over 30 species3.) It is no longer La Trobe University, Bundoora 3083, Victoria, Australia. (Box 2), other aspects of their bireasonable to ignore the effects of ology are more variable. They reCSD on population biology and it semble haploid males very closely has been considered explicitly in several recent studies, in Bracon 1 but are clearly larger ranging from the evolution of signalling to the rearing of para- than haploid males in some other species 7-10. In sawflies, sitoids for biological control. This new synthesis of genetics this large size difference makes it difficult for diploid males and population biology promises to add considerably to our to copulate successfully TMbut this is probably not the case understanding of hymenopteran biology. in most other species. Finally, although Bracon hebetor diploid males have very high larval mortality rates 1, diploid Complementary sex determination and diploid males males of most species appear to have fairly normal viability. Single-locus CSD, which depends on multiple alleles at a The taxonomic distribution of single-locus CSD is poorly single locus (Box 1), was first described in the parasitoid understood (Box 3), but species with single-locus CSD range wasp Bracon hebetoP. Heterozygotes (AiAj) are female while from non-social parasitoid wasps and sawflies to eusocial homozygotes (A.r4i or A.r4j) and hemizygotes (Ai or Aj) are bees and ants. Thus, at least some representatives of each diploid and haploid males, respectivelyL Diploid males pro- of the main hymenopteran lifestyles are subject to the probduce diploid sperm and are effectively sterile (Box 2), im- lem of DMP. It is also clear that there is a strong negative posing a genetic load on the population. In a random-mating correlation between the occurrence of inbreeding and CSD, population with k equally common sex alleles, this genetic presumably because inbreeding increases DMP (Box 2).
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