What is sexual selection and the short herstory of female trait variation

Abstract

Rosvall’s paper links to recent unproductive semantic debates about definitions of sexual selection. Her binning of hypotheses as natural or sexual selection recapitulate the prejudices that have traditionally blinded many investigators to variation among females, on which female–female competition would depend. Perhaps, as a result, she missed some richly predictive long-standing hypotheses of among-female reproductive competition. Nonetheless, I applaud her efforts to increase attention to the biology of females. I remark first on the differences between semantics and hypothetico-deductive logic and then briefly describe three hypotheses of between-female reproductive competition to make the point that what matters is not whether females fit into a bin designed for males but to understand the origins and implications of variation among females. Darwin (1859) anticipated contemporary controversies: “… the manner in which the individuals of either sex or of both sexes are affected through sexual selection cannot fail to be complex in the highest degree (p 296).” The complexities Darwin was talking about lie in the details of any syllogism of selection (any set of assumptions that make up any hypothesis of selection). Darwin’s (1859) least mature published definition of sexual selection was the first narrow sense definition of natural selection (as opposed to artificial selection). Unlike natural selection, which works on phenotypic variation among all individuals of a species, sexual selection has amore narrowed focus acting on variation among individuals within a sex. Thus, sexual selection is as Darwin said, “a type of selection” and he meant natural selection as his topic in 1859 was natural as opposed to artificial selection. He went on to say, “Sexual Selection … depends, not on a struggle for existence, but on a struggle between the males for possession of the females; the result is not death to the unsuccessful competitor, but few or no offspring (page 103).” Darwin’s later 1871 sexual selection hypothesis was his most mature, and it was the first broad sense definition of sexual selection. He said, “Sexual selection … depends on the advantage which certain individuals have over other individuals of the same sex and species, in exclusive relation to reproduction (page 256).” He therewith broadened the scope of mechanism as well as the components of fitness that were acted on via male–male combat. Sexual selection is in fact a narrow-sense syllogism of natural selection, as Darwin (1871) made clear. Selection hypotheses (syllogisms) consist of three kinds of assumptions about: 1) the unit of selection (Lewontin 1970) whose members vary, 2) the environment or social mechanisms that sort among unit members according to their phenotypic variation, and 3) the component of fitness that sorting affects. Imagine a table comparing the required assumptions of a few selection hypotheses. The differences would be instructive if the table arrangement placed types of assumptions from broad (most inclusive) to narrow (increasingly particular). The result would be a series of syllogistic statements with a mixture of broad, comprehensive, and narrow restricted assumptions. If the assumptions are reasonable, they completely describe what must be observed to demonstrate the verity of a particular, given syllogism, that selection hypothesis—by whatever name. And, no matter its name, each would have extraordinary power to inform us about the nature of life when we test them. If the assumptions are met, we will know more about how nature works: 1) Who varies, that is, what units of life (genes, cells, individuals within a sex, all individuals within a population, between populations, between species, etc.) get sorted? 2) How does variation in the social or ecological environment mechanistically sort among individuals? 3) What component(s) of fitness (survival, number of mates, number of bouts of reproduction, number of offspring—at birth or at age of reproduction) is/are affected by the mechanistic sorting? In the few examples that follow, I take an operational approach to describe syllogisms that constitute hypotheses of among-female selection. • Assume 1) female aggressive behavior varies and is induced by threats to female maternity certainty (Gowaty 1981), 2) conspecific nest parasites differentially threaten females’ maternity certainty (Gowaty and Karlin 1984; Gowaty and Bridges 1991), 3) affecting the number of genetic offspring females raise. This is the maternity certainty hypothesis, which predicts that female–female aggression peaks during egg laying, not before egg laying as other hypotheses predicted. Field experiments (Gowaty and Wagner 1988) revealed that female eastern bluebird aggression to conspecific and heterospecific parasites peaked during egg laying consistent with the hypothesis that females fight to protect their genetic maternity, just as males fight to protect their genetic paternity. • Assume 1) females mated to males they do not prefer produce less viable offspring than females mated with males they do prefer (Moore et al. 2003, Bluhm and Gowaty 2004b, Anderson et al. 2007); 2) females mated with males, they do not prefer compensate for offspring viability deficits by laying more eggs than females mated to males they do prefer (Bluhm and Gowaty 2004a; Anderson et al. 2007), 3) resulting in number of offspring at reproductive age being similar for compensating females and those mated with those they prefer (Gowaty et al. 2007). • Assume 1) females vary in ability to raise nestlings without help (Gowaty 1996b); 2) males “helpfully coerce” females (Gowaty 1996a) so that needy females, but not independent females, must trade male help for paternity certainty (Gowaty 1999) so that 3) the number of breeding-age offspring varies because of among-female variation in (1). The female constraint hypothesis (Gowaty and Buschhaus 1998) predicts female extrapair mating behavior, female–female territorial aggression, and fitness variation among females, among males, and offspring as a function of variation in female neediness. The operational approach, as I demonstrate it above, focuses, not on the name of a hypothesis but on the testability of assumptions, the richness of their predictions and ultimately what their tests will reveal about nature. I hope that it will help bring to fruition Rosvall’s excellent goal of spot lighting attention to the biology of females.