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. 2009 May 22;276(1663):1889-97.
doi: 10.1098/rspb.2008.1923. Epub 2009 Feb 25.

Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings

Elise Huchard  1 , Alexandre Courtiol, Julio A Benavides, Leslie A Knapp, Michel Raymond, Guy Cowlishaw
Affiliations

Can fertility signals lead to quality signals? Insights from the evolution of primate sexual swellings

Elise Huchard et al. Proc Biol Sci. .

Abstract

The sexual swellings of female primates have generated a great deal of interest in evolutionary biology. Two hypotheses recently proposed to elucidate their functional significance argue that maximal swelling size advertises either female fertility within a cycle or female quality across cycles. Published evidence favours the first hypothesis, and further indicates that larger swellings advertise higher fertility between cycles. If so, a male preference for large swellings might evolve, driving females to use swellings as quality indicators, as proposed by the second hypothesis. In this paper, we explore this possibility using a combination of empirical field data and mathematical modelling. We first test and find support for three key predictions of the female-quality hypothesis in wild chacma baboons (Papio ursinus): (i) inter-individual differences in swelling size are maintained across consecutive cycles, (ii) females in better condition have larger swellings and higher reproductive success, and (iii) males preferentially choose females with large swellings. We then develop an individual-based simulation model that indicates that females producing larger swellings can achieve higher mating success even when female-female competition is low and within-female variance in the trait is high. Taken together, our findings show that once sexual swellings have evolved as fertility signals, they might, in certain socio-sexual systems, be further selected to act as quality signals. These results, by reconciling two hypotheses, help to clarify the processes underlying sexual swelling evolution. More generally, our findings suggest that mate choice for direct benefits (fertility) can lead to indirect benefits (good genes).

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Figures

Figure 1
Figure 1
Corrected swelling area against female body condition. Corrected swelling area is set for a female from the large troop and corrected for cycle number, age and body size using the parameter estimates of the model. Female condition is measured as the residuals of body mass against body size (crown–rump length). Each circle represents an estimate of the swelling area for one cycle. Estimates for the same female are linked by dotted lines. The line represents the predicted value of the model when the categorical variables are set as described above and the continuous variables are set to the sample average.
Figure 2
Figure 2
Selection intensity for large swellings in relation to breeding synchrony across a range of conditions. The intensity of selection for large swellings is measured as the Pearson correlation coefficient between female mating success and mean maximal swelling size. Breeding synchrony follows a beta distribution, described by two parameters α and β, ranging from total breeding asynchrony (α=β=1) to total breeding synchrony (α=β=∞). The selection intensity for any given level of breeding synchrony was investigated in relation to (a) the relative magnitude of intra-individual variance (denoted varintra) compared with inter-individual variance (denoted varinter) in swelling size (white bars, varintra/varinter=5; light grey bars, varintra/varinter=1; dark grey bars, varintra/varinter=1/5), (b) the number of females per troop (white bars, 5 females; light grey bars, 15 females; dark grey bars, 40 females) and (c) the number of cycles to conception (white bars, two cycles; light grey bars, four cycles; dark grey bars, six cycles). The means and standard errors of the correlation coefficients are shown.
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