Reinterpreting Bateman gradients: multiple mating and selection in both sexes of a songbird species

Abstract

Bateman's principle, which states that male reproductive success should increase with multiple mating, whereas female reproductive success should not, has long been used to explain sex differences in behavior. The statistical relationship between mating success and reproductive success, or Bateman gradient, has been proposed as a way to quantify sex differences in sexual selection. We used a long-term data set on the distribution of paternity in the socially monogamous dark-eyed junco to examine the effect of multiple mating on lifetime reproductive success and to determine the relative contributions of within-pair and extra-pair mating. Both sexes exhibited a strong positive Bateman gradient, even when the number of breeding years was accounted for. Although theory suggests that this pattern indicates a strong potential for sexual selection in both sexes, we argue that the interpretation of strong Bateman gradients, particularly in females, has many potential complications. We discuss several alternative explanations for our results, none of which requires sexual selection acting on female traits, including targeting of inherently fecund females by males seeking extra-pair mates and increased power to detect extra-pair offspring as family size increases. Because neither of these explanations requires that increased mating success causes increased reproductive success, we conclude that using Bateman gradients to measure the potential for sexual selection may be misleading for some mating systems and life histories, such as the iteroparous social monogamy found in juncos.DEPOSIT STATEMENT: This is a pre-copyedited, author-produced PDF of an article accepted for publication in 'Behavioral Ecology' following peer review. The version of record is available online at:10.1093/beheco/ars077.

Bateman's principle is reversed in a cooperatively breeding bird

“…selection on traits used to increase social status or gain access to resources related to reproduction [17]) could still be occurring in this and other cooperatively breeding species, mutual sexual selection seems to be important. Bateman's classic work on Drosophila has recently been challenged [18], and the significance of positive Bateman gradients in females has been questioned [5]. Instead of reflecting selection on females to mate multiply, positive female Bateman gradients could result from males targeting fecund females, the increased likelihood of extra-pair mate detection with increases in brood size, or iteroparous mate resampling [5].…”

“…Bateman's classic work on Drosophila has recently been challenged [18], and the significance of positive Bateman gradients in females has been questioned [5]. Instead of reflecting selection on females to mate multiply, positive female Bateman gradients could result from males targeting fecund females, the increased likelihood of extra-pair mate detection with increases in brood size, or iteroparous mate resampling [5]. Moreover, the phenotypic traits that predict high mating success may be different for males and females even though they can result in similar gradients for both sexes [5], showing that reproductive success in each sex may be subject to different selective pressures and trade-offs [19].…”

“…Instead of reflecting selection on females to mate multiply, positive female Bateman gradients could result from males targeting fecund females, the increased likelihood of extra-pair mate detection with increases in brood size, or iteroparous mate resampling [5]. Moreover, the phenotypic traits that predict high mating success may be different for males and females even though they can result in similar gradients for both sexes [5], showing that reproductive success in each sex may be subject to different selective pressures and trade-offs [19]. However, many of the issues underlying the interpretation of female Bateman gradients may be less of a concern in cooperatively breeding birds because (i) female fecundity is likely to be constrained by available parental care rather than egg production (clutch sizes are relatively small and invariable) and (ii) patterns of mate resampling in a permanent social group will differ from those in a larger population.…”

Polyandry as a mediator of sexual selection before and after mating

“…We agree with Parker & Birkhead [7], who argue that the slopes of the so-called ‘Bateman gradients’ offer key measures because they can, in theory, indicate directly the intensity with which sexual selection operates. However, we recognize that empirical measurement of Bateman gradients in natural populations of animals is not without its problems, and that caution is necessary in interpreting positive slopes as evidence of sexual selection when other measures of the opportunity for selection, or data on selection differentials for traits under selection, are unavailable [13]. Nonetheless, Bateman gradients have considerable heuristic value for the theme of this volume, because they address explicitly how polyandry will influence sexual selection.…”

Greater opportunities for sexual selection in male than in female obligate brood parasitic birds

“…Alternatively, females can have positive Bateman's Gradients and more variability in reproductive success in species with “sex‐role reversal,” in which males provide the majority or all of parental investment (Clutton‐Brock, ; Jones, Rosenqvist, Berglund, Arnold, & Avise, ), as well as in cooperative breeding, with a male‐biased pattern of helping and greater intrasexual competition in females (Apakupakul & Rubenstein, ; Hauber & Lacey, ). By contrast, for species with low initial asymmetry in gametes followed by extensive biparental care, both sexes should be subject to similar and low pressures of sexual selection, although the realized amount of parental care performed by each sex is often difficult to measure (Gerlach, McGlothlin, Parker, & Ketterson, ).…”