Phenology of scramble polygyny in a wild population of chrysomelid beetles: the opportunity for and the strength of sexual selection [corrected]

Abstract

Recent debate has highlighted the importance of estimating both the strength of sexual selection on phenotypic traits, and the opportunity for sexual selection. We describe seasonal fluctuations in mating dynamics of Leptinotarsa undecimlineata (Coleoptera: Chrysomelidae). We compared several estimates of the opportunity for, and the strength of, sexual selection and male precopulatory competition over the reproductive season. First, using a null model, we suggest that the ratio between observed values of the opportunity for sexual selections and their expected value under random mating results in unbiased estimates of the actual nonrandom mating behavior of the population. Second, we found that estimates for the whole reproductive season often misrepresent the actual value at any given time period. Third, mating differentials on male size and mobility, frequency of male fighting and three estimates of the opportunity for sexual selection provide contrasting but complementary information. More intense sexual selection associated to male mobility, but not to male size, was observed in periods with high opportunity for sexual selection and high frequency of male fights. Fourth, based on parameters of spatial and temporal aggregation of female receptivity, we describe the mating system of L. undecimlineata as a scramble mating polygyny in which the opportunity for sexual selection varies widely throughout the season, but the strength of sexual selection on male size remains fairly weak, while male mobility inversely covaries with mating success. We suggest that different estimates for the opportunity for, and intensity of, sexual selection should be applied in order to discriminate how different behavioral and demographic factors shape the reproductive dynamic of populations.

Figure 1. Mating and oviposition in L. undecimlineata.

Male and gravid female in copula (notice aedeagus intromission) next to a batch of eggs recently laid by the female under a leaf of the host plant Solanum lanceolatum.

Figure 2. Number of daily observed copulating females in a population of L. undecimlineata.

Observations were carried out between July 21 (day 0) and November 7 (day 95), 2004. Dashed lines define four 20-day periods between days 6 and 85 (in which the first and last mating couples were observed), used to analyze temporal fluctuation in the reproductive dynamics of the population.

Figure 3. Male and female abundance over the mating season of L. undecimlineata.

Number of males (shaded boxes) and females (open boxes) per plant observed over the four periods of the mating season (n = 20 days in all periods). Median, quartiles and extreme values are represented. Males are significantly more abundant than females overall, and this difference is significantly greater in period 2 (Table 1).

Figure 4. The strength of sexual selection in L. undecimlineata.

Standardized mating differentials (m’) and bootstrap 95% confidence intervals for male size (A) and mobility (B) in each period and the whole reproductive season. None of the standardized mating differentials on male size differed from random expectations (dashed horizontal line at y = 0) in any period or the whole season. Male mobility (plants occupied per day observed) showed negative values significantly different from random expectations in periods 2 and 3, and the whole season. Males that moved less had higher mating success.

Figure 5. Spatial and temporal female crowding in L. undecimlineata.

Estimates and bootstrap 95% confidence intervals of average mating success (mated females per successful male, m), number of mated females per time period (t), mean spatial female crowding around males (m*) and mean temporal female crowding (t*) in each period (squares) and for the whole season (circles). A–D) observed values (open markers) and values expected under random mating (solid markers). E–H) the ratio between observed and randomly expected values (O/RE) from the null model of each estimate. The dashed horizontal lines at y = 1 represent no difference between observed and randomly expected values (O/RE  = 1).

Figure 6. Variance in male mating success in L. undecimlineata.

Estimates and bootstrap 95% confidence intervals of variance in mating success among successful males (V _harem) and among all males (V _mates) in each period (squares) and for the whole season (circles). A–D) observed values (open markers) and values expected under random mating (solid markers). E–H) the ratio between observed and randomly expected values (O/RE) from the null model of each estimate. The dashed horizontal lines at y = 1 represent no difference between observed and randomly expected values (O/RE  = 1). Variances in male mating success among successful males (V _harem), and among all males (V _mates) were significantly higher than expected under random mating for period 2, barely higher for period 1, and not different or even significantly lower than random expectations in period 3.

Figure 7. The opportunity for sexual selection in L. undecimlineata.

Estimates and bootstrap 95% confidence intervals of the opportunity for sexual selection among successful males (I _harem), the opportunity for sexual selection (I _mates) derived from the relationship between the number of mated females per successful male (m), the variance in mating success among successful males (V _harem) and among all males (V _mates); its value adjusted (I _mates(adj)) to sex ratio (R) mean spatial female crowding around males (m*), and the opportunity for sexual selection derived from female receptive phenology (I _mates(phen)) in each period (squares) and for the whole season (circles). A–D) observed values (open markers) and values expected under random mating (solid markers). E–H) the ratio between observed and randomly expected values (O/RE) from the null model of each estimate. The dashed horizontal lines at y = 1 represent no difference between observed and randomly expected values (O/RE  = 1). All four estimates of I for period 2, and two (I _mates(adj) and I _mates(phen)) for period 3, are significantly higher than random expectations. The opportunity for sexual selection for both estimates that factor in sex ratio (I _mates(adj) and I _mates(phen)) resulted in significantly higher randomly expected values for periods 1, 2 and 3. Relatively fewer mating events in period 4 due to lower density in the population and a decrease in reproductive behavior resulted in much larger confidence intervals.

Figure 8. Quantitative characterization of the mating system of L. undecimlineata.

The relationship between female mean crowding around males (m*), in time (t*), and I _mates for each period (1 in orange, 2 in red, 3 in blue and 4 in green) and the whole season (T in black). Orthogonal lines and projected squares represent bootstrap 95% confidence intervals for each value. A) Observed values following Shuster & Wade (, pages 92, 93). Arrows represent the temporal trajectory of the mating system throughout the season. High values of m* and t* in period 2 correspond with high values of I _mates. B) The ratio between observed and randomly expected values (O/RE). The dashed horizontal lines at y = 1 in all planes represents no difference between observed and randomly expected values (O/RE  = 1). Only the difference of I _mates between periods 2 and 3 is significant, while only the values for period 2 and the whole season are significantly higher than random expectations.

Figure 9. Covariance across temporal intervals in male mating success and sex ratio in L. undecimlineata.

Observed values represented by open markers, randomly expected values represented by solid markers, 95% bootstrap confidence intervals represented by lines and random expectations represented by dashed horizontal line at y = 0. A) Covariance across temporal intervals in male mating success which includes the temporal and spatial variation of sex ratio (Cov _(phen) ×10⁻²). Only the observed value for period 4 differed from random expectations although no differences were observed among periods or to the whole season. B) Sex ratio (R), the number of receptive females to total males; there were no significant differences among periods while the value for the whole season was significantly different from periods 3 and 4.

Figure 10. Male fighting in L. undecimlieneata.

Fighter (A) and fight (B) frequency throughout the reproductive season (n = 20 days in all periods). Median, quartiles and extreme values are represented. Both the number of fighters and fight frequency peaked in period 2 (Tables 3,4).