Within-group male relatedness reduces harm to females in Drosophila

Journal name:
Nature
Volume:
505,
Pages:
672–675
Date published:
DOI:
doi:10.1038/nature12949
Received
Accepted
Published online

To resolve the mechanisms that switch competition to cooperation is key to understanding biological organization1. This is particularly relevant for intrasexual competition, which often leads to males harming females2. Recent theory proposes that kin selection may modulate female harm by relaxing competition among male relatives3, 4, 5. Here we experimentally manipulate the relatedness of groups of male Drosophila melanogaster competing over females to demonstrate that, as expected, within-group relatedness inhibits male competition and female harm. Females exposed to groups of three brothers unrelated to the female had higher lifetime reproductive success and slower reproductive ageing compared to females exposed to groups of three males unrelated to each other. Triplets of brothers also fought less with each other, courted females less intensively and lived longer than triplets of unrelated males. However, associations among brothers may be vulnerable to invasion by minorities of unrelated males: when two brothers were matched with an unrelated male, the unrelated male sired on average twice as many offspring as either brother. These results demonstrate that relatedness can profoundly affect fitness through its modulation of intrasexual competition, as flies plastically adjust sexual behaviour in a manner consistent with kin-selection theory.

At a glance

Figures

  1. The effect of male-male relatedness on female fitness.
    Figure 1: The effect of male–male relatedness on female fitness.

    a, Female lifetime reproductive success was higher in the high male-relatedness treatment (AAA) than in the low male-relatedness treatment (ABC; F1, 119 = 4.11, P = 0.045). This difference was highly significant when we included female reproductive lifespan and its interaction with treatment as factors in the analysis (F1,117 = 20.83, P<0.001). b, Female reproductive lifespan was longer in the high-male relatedness treatment (AAA) than in the low-male relatedness treatment (ABC; F1,119 = 6.55, P = 0.012) and the probability to cease reproducing at any given time was lower (χ22 = 3.95, P = 0.047; nAAA = 63, nABC = 62). c, Female reproductive rates declined more sharply in individual females exposed to ABC rather than to AAA males (average number of offspring produced by AAA and ABC females over successive days of their life: treatment, χ21 = 4.11, P = 0.043; day, χ21 = 1570.8, P<0.001; treatment–day interaction, χ21 = 7.55, P = 0.006). d, Offspring viability (egg-to-adult survival) declined more sharply over time in females exposed to ABC rather than AAA males (treatment–week interaction: χ21 = 9.23, P = 0.002, estimated difference in viability drop AAA–ABC, mean±s.e.m.: estimate = −0.231±0.075). Error bars represent mean ±s.e.m.; *P < 0.05; nAAA = 61, nABC = 60 unless stated otherwise.

  2. The effect of male-male relatedness on male sexual behaviour and longevity.
    Figure 2: The effect of male–male relatedness on male sexual behaviour and longevity.

    a, Triplets of unrelated males (ABC) had a significantly higher frequency of male–male fighting than triplets of brothers (AAA) (proportion of focal scans in which male–male fighting was observed, χ22 = 14.46, P<0.001; Tukey, ABC–AAA, z = 3.73, P<0.001, ABC–AAB, z = 2.92, P = 0.01, nAAA = 47, nAAB = 47, nABC = 45). b, Compared to triplets of brothers (AAA), triplets of unrelated males (ABC) were characterized by higher courting intensity (that is, number of courting males when courting was observed, χ22 = 5.01, P = 0.081; Tukey ABC–AAA: z = 2.38, P = 0.045; nAAA = 47, nAAB = 47, nABC = 45). c, Male longevity was significantly lower in unrelated triplets (ABC) than among full-sibling brothers (AAA; F2, 128 = 3.77, P = 0.026; estimated differential lifespan for ABC, mean±s.e.m.: −5.62±2.63, t = −2.139, P = 0.034; nAAA = 43, nAAB = 44, nABC = 45). d, We found significant differences in male mortality risk across treatments (χ22 = 10.47, P = 0.005), and post-hoc direct comparisons between the treatments indicated that this effect was due to males in unrelated triplets (ABC) being more likely to die than in AAA triplets (χ22 = 9.55, P = 0.002) and AAB triplets (χ22 = 6.66, P = 0.010; nAAA = nAAB = nABC = 47). Error bars represent mean ±s.e.m.; asterisks represent significant post-hoc comparisons. *P < 0.05.

  3. Unrelated males outcompete brothers.
    Figure 3: Unrelated males outcompete brothers.

    Proportion of offspring sired by the unrelated male (B) in male triplets in which two brothers were matched with an unrelated male (AAB, n = 54). The B male sired on average half of the offspring produced by the female, with the two brothers siring the other half between them. This distribution of paternity deviated significantly from an equalitarian distribution of paternity across the three males (that is, 0.33; z = 3.99, P<0.001), and was independent of male stock (that is, se, spa). Error bar represents mean ±s.e.m.

  4. Extended Data Fig. 1:

    a, Rate-sensitive estimates of individual female fitness (wind) over a gradient in population growth rates (r). Female fitness was estimated to be higher under high within-group male relatedness for values of r ranging from −0.1 to 0 (dark shaded area), a similar non-significant (0.05 < P<0.08) pattern was extended for r = −0.2 and r = 0.1 (light shaded area). b, The effect of within-group male relatedness on population fitness. The relative fitness cost of reducing within-group male relatedness at different population growth rates (r). The dashed line identifies relative fitness of 1, where reduction in within-group male relatedness has no fitness cost. Reducing within-group male relatedness is always costly over the range of population growth rates explored, but particularly so with smaller growth rates.

Tables

  1. Female rate-insensitive fitness measures in experiment 2
    Extended Data Table 1: Female rate-insensitive fitness measures in experiment 2
  2. Female post-mating responses in experiment 3
    Extended Data Table 2: Female post-mating responses in experiment 3
  3. Summary of statistical tests in experiment 4
    Extended Data Table 3: Summary of statistical tests in experiment 4
  4. Effect of genotype of A male and genotype of B male on the response variable
    Extended Data Table 4: Effect of genotype of A male and genotype of B male on the response variable

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Author information

  1. These authors contributed equally to this work.

    • Pau Carazo &
    • Cedric K. W. Tan

Affiliations

  1. Edward Grey Institute, Department of Zoology, University of Oxford, Oxford OX1 3PS, UK

    • Pau Carazo,
    • Cedric K. W. Tan,
    • Felicity Allen,
    • Stuart Wigby &
    • Tommaso Pizzari

Contributions

Experiment 1 was designed by P.C., S.W. and T.P., conducted by P.C. and F.A., and analysed by P.C. Experiment 2 was designed by P.C., C.K.W.T., S.W. and T.P., and conducted and analysed by P.C. Experiment 3 was designed and conducted by S.W. and P.C., and analysed by P.C. Experiment 4 was designed by C.K.W.T., T.P. and S.W., and conducted and analysed by C.K.W.T. The article was conceived and written by T.P. with input from P.C., C.K.W.T. and S.W.

Competing financial interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to:

Data have been deposited in the Dryad Digital Repository at http://dx.doi.org/10.5061/dryad.9c7bq .

Author details

Extended data figures and tables

Extended Data Figures

  1. Extended Data Figure 1: (59 KB)

    a, Rate-sensitive estimates of individual female fitness (wind) over a gradient in population growth rates (r). Female fitness was estimated to be higher under high within-group male relatedness for values of r ranging from −0.1 to 0 (dark shaded area), a similar non-significant (0.05 < P<0.08) pattern was extended for r = −0.2 and r = 0.1 (light shaded area). b, The effect of within-group male relatedness on population fitness. The relative fitness cost of reducing within-group male relatedness at different population growth rates (r). The dashed line identifies relative fitness of 1, where reduction in within-group male relatedness has no fitness cost. Reducing within-group male relatedness is always costly over the range of population growth rates explored, but particularly so with smaller growth rates.

Extended Data Tables

  1. Extended Data Table 1: Female rate-insensitive fitness measures in experiment 2 (70 KB)
  2. Extended Data Table 2: Female post-mating responses in experiment 3 (58 KB)
  3. Extended Data Table 3: Summary of statistical tests in experiment 4 (140 KB)
  4. Extended Data Table 4: Effect of genotype of A male and genotype of B male on the response variable (74 KB)

Additional data