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Mother knows best: dominant females determine offspring dispersal in red foxes (Vulpes vulpes).

Whiteside HM, Dawson DA, Soulsbury CD, Harris S - PLoS ONE (2011)

Bottom Line: Males with dominant mothers dispersed significantly more often than males with subordinate mothers, whereas dispersing females were significantly more likely to have subordinate mothers compared to philopatric females.Male dispersal may be driven by inbreeding avoidance, whereas female dispersal appears to be influenced by the fitness advantages associated with residing with the same-sex dominant parent.Selection pressure for paternal influence on offspring dispersal is low due to the limited costs associated with retaining unrelated males and the need for alternative inbreeding avoidance mechanisms between the dominant male and his female offspring.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Bristol, Bristol, United Kingdom. Helen.Whiteside@Bristol.ac.uk

ABSTRACT

Background: Relatedness between group members is central to understanding the causes of animal dispersal. In many group-living mammals this can be complicated as extra-pair copulations result in offspring having varying levels of relatedness to the dominant animals, leading to a potential conflict between male and female dominants over offspring dispersal strategies. To avoid resource competition and inbreeding, dominant males might be expected to evict unrelated males and related females, whereas the reverse strategy would be expected for dominant females.

Methodology/principal findings: We used microsatellites and long-term data from an urban fox (Vulpes vulpes) population to compare dispersal strategies between offspring with intra- and extra-group fathers and mothers of differing social status in red foxes. Relatedness to the dominant male had no effect on dispersal in offspring of either sex, whereas there was a strong effect of relatedness to resident females on offspring dispersal independent of population density. Males with dominant mothers dispersed significantly more often than males with subordinate mothers, whereas dispersing females were significantly more likely to have subordinate mothers compared to philopatric females.

Conclusions/significance: This is the first study to demonstrate that relatedness to resident females is important in juvenile dispersal in group-living mammals. Male dispersal may be driven by inbreeding avoidance, whereas female dispersal appears to be influenced by the fitness advantages associated with residing with the same-sex dominant parent. Selection pressure for paternal influence on offspring dispersal is low due to the limited costs associated with retaining unrelated males and the need for alternative inbreeding avoidance mechanisms between the dominant male and his female offspring. These findings have important implications for the evolution of dispersal and group living in social mammals, and our understanding of a key biological process.

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Frequency of dispersing and philopatric red fox offspring from parents of differing social status.Paternal group association is shown for male offspring (A) and female offspring (B). Maternal social status is shown for male offspring (C) and female offspring (D). Maternal social status had a sex-dependent influence on offspring dispersal, whereas the father's social group had no effect.
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pone-0022145-g001: Frequency of dispersing and philopatric red fox offspring from parents of differing social status.Paternal group association is shown for male offspring (A) and female offspring (B). Maternal social status is shown for male offspring (C) and female offspring (D). Maternal social status had a sex-dependent influence on offspring dispersal, whereas the father's social group had no effect.

Mentions: Only foxes with known dispersal status and assigned parents with established social status and/or extra-group paternity could be analyzed; thus 24% of all cubs captured between 1998 and 2009 were used (Table 3). Paternity did not affect male (Fig. 1A, p = 1, N = 19) or female (Fig. 1B, p = 0.378, N = 22) offspring dispersal, whereas maternity did. Males with dominant mothers dispersed significantly more often than males with subordinate mothers (Fig. 1C, p<0.001, N = 25). In contrast, dispersing females were significantly more likely to have subordinate mothers compared to philopatric females (Fig. 1D, p<0.001, N = 27). Analyzed separately, the high-density samples showed the same pattern. Paternity did not have an effect on offspring dispersal for males (p = 0.070, N = 13) or females (p = 0.999, N = 17), whereas maternity significantly affected male (p = 0.004, N = 18) and female (p<0.001, N = 22) dispersal. Low-density samples showed a similar trend but samples sizes were too low (N = 24) for statistical analysis. Only two cubs with known dispersal status were assigned subordinate fathers. They followed the expected dispersal strategies if maternal social status affects juvenile dispersal: a male with a dominant mother dispersed, a male with a subordinate mother was philopatric.


Mother knows best: dominant females determine offspring dispersal in red foxes (Vulpes vulpes).

Whiteside HM, Dawson DA, Soulsbury CD, Harris S - PLoS ONE (2011)

Frequency of dispersing and philopatric red fox offspring from parents of differing social status.Paternal group association is shown for male offspring (A) and female offspring (B). Maternal social status is shown for male offspring (C) and female offspring (D). Maternal social status had a sex-dependent influence on offspring dispersal, whereas the father's social group had no effect.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3140410&req=5

pone-0022145-g001: Frequency of dispersing and philopatric red fox offspring from parents of differing social status.Paternal group association is shown for male offspring (A) and female offspring (B). Maternal social status is shown for male offspring (C) and female offspring (D). Maternal social status had a sex-dependent influence on offspring dispersal, whereas the father's social group had no effect.
Mentions: Only foxes with known dispersal status and assigned parents with established social status and/or extra-group paternity could be analyzed; thus 24% of all cubs captured between 1998 and 2009 were used (Table 3). Paternity did not affect male (Fig. 1A, p = 1, N = 19) or female (Fig. 1B, p = 0.378, N = 22) offspring dispersal, whereas maternity did. Males with dominant mothers dispersed significantly more often than males with subordinate mothers (Fig. 1C, p<0.001, N = 25). In contrast, dispersing females were significantly more likely to have subordinate mothers compared to philopatric females (Fig. 1D, p<0.001, N = 27). Analyzed separately, the high-density samples showed the same pattern. Paternity did not have an effect on offspring dispersal for males (p = 0.070, N = 13) or females (p = 0.999, N = 17), whereas maternity significantly affected male (p = 0.004, N = 18) and female (p<0.001, N = 22) dispersal. Low-density samples showed a similar trend but samples sizes were too low (N = 24) for statistical analysis. Only two cubs with known dispersal status were assigned subordinate fathers. They followed the expected dispersal strategies if maternal social status affects juvenile dispersal: a male with a dominant mother dispersed, a male with a subordinate mother was philopatric.

Bottom Line: Males with dominant mothers dispersed significantly more often than males with subordinate mothers, whereas dispersing females were significantly more likely to have subordinate mothers compared to philopatric females.Male dispersal may be driven by inbreeding avoidance, whereas female dispersal appears to be influenced by the fitness advantages associated with residing with the same-sex dominant parent.Selection pressure for paternal influence on offspring dispersal is low due to the limited costs associated with retaining unrelated males and the need for alternative inbreeding avoidance mechanisms between the dominant male and his female offspring.

View Article: PubMed Central - PubMed

Affiliation: School of Biological Sciences, University of Bristol, Bristol, United Kingdom. Helen.Whiteside@Bristol.ac.uk

ABSTRACT

Background: Relatedness between group members is central to understanding the causes of animal dispersal. In many group-living mammals this can be complicated as extra-pair copulations result in offspring having varying levels of relatedness to the dominant animals, leading to a potential conflict between male and female dominants over offspring dispersal strategies. To avoid resource competition and inbreeding, dominant males might be expected to evict unrelated males and related females, whereas the reverse strategy would be expected for dominant females.

Methodology/principal findings: We used microsatellites and long-term data from an urban fox (Vulpes vulpes) population to compare dispersal strategies between offspring with intra- and extra-group fathers and mothers of differing social status in red foxes. Relatedness to the dominant male had no effect on dispersal in offspring of either sex, whereas there was a strong effect of relatedness to resident females on offspring dispersal independent of population density. Males with dominant mothers dispersed significantly more often than males with subordinate mothers, whereas dispersing females were significantly more likely to have subordinate mothers compared to philopatric females.

Conclusions/significance: This is the first study to demonstrate that relatedness to resident females is important in juvenile dispersal in group-living mammals. Male dispersal may be driven by inbreeding avoidance, whereas female dispersal appears to be influenced by the fitness advantages associated with residing with the same-sex dominant parent. Selection pressure for paternal influence on offspring dispersal is low due to the limited costs associated with retaining unrelated males and the need for alternative inbreeding avoidance mechanisms between the dominant male and his female offspring. These findings have important implications for the evolution of dispersal and group living in social mammals, and our understanding of a key biological process.

Show MeSH
Related in: MedlinePlus