Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance

Crean, Angela J., Dwyer, John M. and Marshall, Dustin J. (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology, 94 11: 2575-2582. doi:10.1890/13-0184.1

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Author Crean, Angela J.
Dwyer, John M.
Marshall, Dustin J.
Title Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance
Journal name Ecology   Check publisher's open access policy
ISSN 0012-9658
1939-9170
Publication date 2013-01-01
Year available 2013
Sub-type Article (original research)
DOI 10.1890/13-0184.1
Open Access Status File (Publisher version)
Volume 94
Issue 11
Start page 2575
End page 2582
Total pages 8
Place of publication Ithaca, NY, United States
Publisher Ecological Society of America
Language eng
Abstract The ability of females to adaptively influence offspring phenotype via maternal effects is widely acknowledged, but corresponding nongenetic paternal effects remain unexplored. Males can adjust sperm phenotype in response to local conditions, but the transgenerational consequences of this plasticity are unknown. We manipulated paternal density of a broadcast spawner (Styela plicata, a solitary ascidean) using methods shown previously to alter sperm phenotype in the field, then conducted in vitro fertilizations that excluded maternal effects and estimated offspring performance under natural conditions. Offspring sired by males from low-density experimental populations developed faster and had a higher hatching success than offspring sired by males living in high densities. In the field, offspring survived relatively better when their environment matched their father's, raising the possibility that fathers can adaptively influence the phenotype of their offspring according to local conditions. As the only difference between offspring is whether they were artificially fertilized by sperm from males kept in high- vs. low-density cages, we can unequivocally attribute any differences in offspring performance to an environmentally induced paternal effect. Males of many species manipulate the phenotype of their sperm in response to sperm competition: our results show this plasticity can influence offspring fitness, potentially in adaptive ways, raising the possibility that adaptive nongenetic paternal effects may be more common than previously thought.
Formatted abstract
The ability of females to adaptively influence offspring phenotype via maternal effects is widely acknowledged, but corresponding nongenetic paternal effects remain unexplored. Males can adjust sperm phenotype in response to local conditions, but the transgenerational consequences of this plasticity are unknown. We manipulated paternal density of a broadcast spawner (Styela plicata, a solitary ascidean) using methods shown previously to alter sperm phenotype in the field, then conducted in vitro fertilizations that excluded maternal effects and estimated offspring performance under natural conditions. Offspring sired by males from low-density experimental populations developed faster and had a higher hatching success than offspring sired by males living in high densities. In the field, offspring survived relatively better when their environment matched their father's, raising the possibility that fathers can adaptively influence the phenotype of their offspring according to local conditions. As the only difference between offspring is whether they were artificially fertilized by sperm from males kept in high- vs. low-density cages, we can unequivocally attribute any differences in offspring performance to an environmentally induced paternal effect. Males of many species manipulate the phenotype of their sperm in response to sperm competition: our results show this plasticity can influence offspring fitness, potentially in adaptive ways, raising the possibility that adaptive nongenetic paternal effects may be more common than previously thought. 
Keyword External fertilization
Nongenetic inheritance
Parental effect
Paternal effect
Sperm phenotype
Sperm plasticity
Styela plicata
Q-Index Code C1
Q-Index Status Confirmed Code
Institutional Status UQ

Document type: Journal Article
Sub-type: Article (original research)
Collections: Official 2014 Collection
School of Biological Sciences Publications
 
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Created: Tue, 03 Dec 2013, 10:54:53 EST by System User on behalf of School of Biological Sciences