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Reproductive Compensation

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Reproductive Compensation doi:10.1111/j.1420-9101.2008.01559.x Reproductive compensation PATRICIA ADAIR GOWATY Department of Ecology and Evolutionary Biology, 621 Charles E. Young Drive, University of California, Los Angeles 90095, USA and The Smithsonian Tropical Research Institute, Unit 0948, APO AA 34002-0948, USA Keywords: Abstract constraints; The reproductive compensation hypothesis says that individuals constrained differential allocation hypothesis; by ecological or social forces to reproduce with partners they do not prefer dispersal limitation; compensate for likely offspring viability deficits. The reproductive compensa- life history trade-offs; tion hypothesis assumes that (i) pathogens and parasites evolve more rapidly mate preferences; than their hosts, (ii) mate preferences predict variation in health and viability offspring viability selection; of offspring, (iii) social and ecological factors keep some individuals from phenotypic plasticity; mating with their preferred partners (some are constrained to mate with sexual coercion. partners they do not prefer), (iv) all individuals may be induced to compensate, so that (v) variation in compensation is due to environmental and developmental factors affecting between-individual abilities to express compensatory mechanisms. Selection favouring compensation may act through variation in prezygotic physiological mechanisms, zygotic mecha- nisms, or parental care to eggs or young that enhance offspring health, increasing the likelihood that some offspring survive to reproductive age, often at a survival cost to the parents. Compensation may be through increased number of eggs laid or offspring born, a compensatory effort working during a single reproductive bout that sometimes will match the number of offspring surviving to reproductive age produced by unconstrained parents during the same bout. The reproductive compensation hypothesis therefore predicts trade-offs in components of fitness for breeders, such that parents constrained to mating with a nonpreferred partner, but who compensate sometimes match their current productivity (number of offspring at reproductive age) to unconstrained parents (those breeding with their preferred partners), and, when all else is equal, die faster than unconstrained parents. The reproductive compensation hypothesis emphasizes that reproductive competition is not just between constrained and unconstrained individuals, but also among con- strained individuals who do and do not compensate. The reproductive compensation hypothesis may thus explain previously unexplained between-population and within-population, between-individual variation in reproductive success, survival, physiology and behaviour. coerced reproduction leads to lower fitness than repro- Introduction duction with preferred partners, whenever heritable But if you try sometimes you might find, You get what you variation (in genes, epigenetic elements, other develop- need mental programmes, etc.) exists, selection will result The Rolling Stones in individuals sensitive to fitness outcomes and able What do individuals do when they are constrained to to flexibly resist mating and reproduction with non- reproduce with nonpreferred partners? If constrained or preferred partners. But, there are situations in which reproduction with nonpreferred partners is the only Correspondence: Patricia Adair Gowaty, Department of Ecology & Evolu- option (Gowaty, 1997). The question then becomes, tionary Biology, University of California, Los Angeles, California 90095, USA. what can individuals – constrained to mate with partners Tel.: 310 206-2186; fax: 310 206-0484; they do not prefer – do, if anything, to make up likely e-mail: [email protected] fitness deficits compared with those individuals mating ª 2008 THE AUTHOR. J. EVOL. BIOL. JOURNAL COMPILATION ª 2008 EUROPEAN SOCIETY FOR EVOLUTIONARY BIOLOGY 1 2 P. A. GOWATY with individuals they do prefer? One possibility is that parasites (Van Valen, 1973). (ii) Variation in offspring constrained individuals attempt to compensate for pre- viability favours mate preferences in both sexes (Bondu- dictable fitness deficits in their offspring (Foerster et al., riansky, 2001; Gowaty & Hubbell, 2005). (iii) Impedi- 2003; Gowaty, 2003; Bluhm & Gowaty, 2004a; Navara ments (ecological and social) to reproduction with one’s et al., 2006; Byers & Waits, 2006; Anderson et al., 2007; best partner exist (see references above). (iv) Mecha- Gowaty et al., 2007). nisms of compensation evolve rapidly to fixation, so that Thinking about some of the ways reproduction may all individuals may compensate and (v) variation in occur under social constraints on female mate prefer- expressed mechanisms of compensation is due primarily ences inspired the reproductive compensation hypothesis to environmental and developmental factors affecting (Gowaty, 1996, 2003; Gowaty & Buschhaus, 1998), but it individual ability to express compensatory mechanisms. is important to keep in mind that reproductive compen- sation can be induced by ecological constraints on mating The Red Queen’s challenge to parents, mate with one’s best (preferred) partner for offspring viability, preferences and constraints on mate preferences such as dispersal limitation and demographic stochastic- ity, not just social constraints. Known social constraints As the metaphor of the Red Queen stresses, pathogens acting on males and females include male–male compet- evolve more rapidly than their hosts. This means that the itive contests, and in some species in which females are pathogens that attack the parental generation may not be invulnerable to social coercion, female mate choice may the same pathogens challenging the health of offspring. limit males’ options for mating partners. Sexually As Hamilton & Zuk (1982) said, if host–parasite cycles of coercive constraints limit females access to partners, but evolutionary response ‘‘are very short, then trying to also males’ and include infanticide (Hrdy, 1974, 1977, choose mates for the ‘right’ genes for resistance is a 1979, 1981), forced copulation (Brownmiller, 1975; perverse task’’ (p. 384). In this case it would be unlikely Cheng et al., 1982, 1983; McKinney et al., 1983; Gowaty that elaborate traits in potential fathers signalled ‘good & Buschhaus, 1998), male aggression against females genes’ for offspring health. If variation in the underlying (Smuts, 1992, 1995; Smuts & Smuts, 1993), male mate- genetic components of offspring viability favour mate guarding (Dickemann, 1979a,b, 1981; Gowaty, 1996), preferences as the reproductive compensation hypothesis sperm plugs and peptides that decrease females’ assumes, there is unlikely to be a single best male, better re-mating tendencies (Chapman et al., 1994; Chapman for all females than any other male, because females & Partridge, 1996; Rice, 1996). vary, and like males, contribute to the genetics, (as well The reproductive compensation hypothesis emphasizes as the epigenetics, ecology, development and culture) of how selection might act not just among constrained and offspring viability. If indicator traits show the true health not constrained individuals, but between constrained status of the signaller, they may be honest indicators of individuals who can and cannot trade-off components of an individuals’ ability to provide direct benefits to fitness to flexibly adjust physiology and behaviour in females and to their offspring, but still say little about ways that enhance the future survival of their offspring. the genetics and development of offspring immune The reproductive compensation hypothesis is sexually systems that must be an important component of symmetric, predicting that both sexes of parent are offspring viability – unless there is little or no evolution sensitive to, can assess, and respond flexibly to environ- of pathogens between parental and offspring generations. mental and social conditions, i.e. both sexes may However, if offspring viability is influenced by alleles that compensate. This paper contains a brief review of the work against offspring generation pathogens, the current assumptions of the reproductive compensation hypo- health status of a potential mate may not predict the thesis, first presented in Gowaty (1996, 2003); Gowaty & health of offspring. In such cases, it is possible that Buschhaus (1998), and Gowaty et al. (2007). It also ‘honest’ indicators manipulate or dazzle choosers, contains a quantitative description of components of exploiting their pre-existing sensory biases (West-Eber- fitness essential for understanding the reproductive hard, 1979, 1984), so that choosers make reproductive compensation hypothesis, a comparison with the differ- decisions that may not favour offspring health. Thus, ential allocation hypothesis, and a discussion of the range showy and elaborate traits could be simultaneously of predictions of the reproductive compensation hypo- honest about some components of fitness (e.g. the thesis with a focus on tests that depend on components of breeders’ current health and ⁄ or probability of survival), fitness. Last, I include a discussion of the question, ‘Can but may provide limited or no information relevant to compensation evolve?’ other components of fitness. This perspective emphasizes that there may be other effects of host–pathogen arms races on individuals’ reproductive decisions besides the The assumptions evolution of elaborate traits in males. Of central impor- The assumptions of the reproductive compensation tance here is that the perennial evolutionary arms races hypothesis
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