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

Authors: Angela J Crean, John M Dwyer and Dustin J Marshall

Published in: Ecology, volume 94, issue 11 (November 2013)

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.

Full paper

Crean AJ, Dwyer JM, Marshall DJ (2013) Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance. Ecology, 94(11): 2575–2582 PDFPDF 493 KB doi:10.1890/13-0184.1

Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance

Authors: Angela J Crean, John M Dwyer and Dustin J Marshall

Published in: PLoS ONE, volume 7, issue 11, doi: 10.1371/journal.pone.0049167

Abstract

Styela plicata larvae

Styela plicata larvae. Image courtesy of Bronwyn Galletly.

Sperm are the most diverse cell type known: varying not only among- and within- species, but also among- and within- ejaculates of a single male.

Recently, the causes and consequences of variability in sperm phenotypes have received much attention, but the importance of within-ejaculate variability remains largely unknown.

Correlative evidence suggests that reduced within-ejaculate variation in sperm phenotype increases a male’s fertilization success in competitive conditions; but the transgenerational consequences of within-ejaculate variation in sperm phenotype remain relatively unexplored.

Here we examine the relationship between sperm longevity and offspring performance in a marine invertebrate with external fertilization, Styela plicata. Offspring sired by longer-lived sperm had higher performance compared to offspring sired by freshly-extracted sperm of the same ejaculate, both in the laboratory and the field. This indicates that within-ejaculate differences in sperm longevity can influence offspring fitness – a source of variability in offspring phenotypes that has not previously been considered. Links between sperm phenotype and offspring performance may constrain responses to selection on either sperm or offspring traits, with broad ecological and evolutionary implications.

Full paper

Crean AJ, Dwyer JM, Marshall DJ (2012) Fertilization is not a new beginning: the relationship between sperm longevity and offspring performance. PLoS ONE 7 (11) PDFPDF 254 KB External linkFull text, doi: 10.1371/journal.pone.0049167