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

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.

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

“…The sire population appeared important to survival in sea bass, supporting recent evidence for a paternal role in increased survival of young fish (Álvarez & Garcia‐Vazquez, 2011; Bang, Grønkjaer, Clemmesen, & Høie, 2006; Rideout, Trippel, & Litvak, 2004), but also other broadcast marine spawners ( Styela plicata ; Crean, Dwyer, & Marshall, 2013). A paternal influence was formerly shown for female hatching rate in sea bass, but not for survival (Ky et al., 2012; Saillant et al., 2001).…”

Ocean acidification impacts on sperm mitochondrial membrane potential bring sperm swimming behaviour near its tipping point

“…A similar study on C. rodgersii, however, found inhibitory effects of both near-and far-future ocean acidification (ΔpH −0.3 and −0.5, respectively) on sperm swimming behaviour (Schlegel et al, in review). These differences may have arisen because responses -and hence gamete quality -can vary with collection date (Table 1) and/or parental experience (Crean et al, 2013;Jensen et al, 2014). Differences in parental genotypes and environments can directly affect gamete plasticity and performance (Crean et al, 2013;Crean and Marshall, 2008;Jensen et al, 2014).…”

“…These differences may have arisen because responses -and hence gamete quality -can vary with collection date (Table 1) and/or parental experience (Crean et al, 2013;Jensen et al, 2014). Differences in parental genotypes and environments can directly affect gamete plasticity and performance (Crean et al, 2013;Crean and Marshall, 2008;Jensen et al, 2014). A similar robustness to climate change has been found in the gene network of the urchin Strongylocentrotus purpuratus (Runcie et al, 2012): elevated seawater temperatures caused perturbations of regulatory genes, which were buffered effectively within the network and did not affect the expression of regulated genes.…”

Environmentally induced (co)variance in sperm and offspring phenotypes as a source of epigenetic effects

“…In a follow-up study to their earlier work (Crean and Marshall, 2008), Crean and colleagues (Crean et al, 2013) explored the consequences of gamete plasticity for offspring. They (Crean et al, 2013) took advantage of the life histories of external fertilisers, dividing sperm and eggs from single individuals before conducting in vitro fertilisations, thereby excluding potentially confounding maternal effects.…”

“…In a follow-up study to their earlier work (Crean and Marshall, 2008), Crean and colleagues (Crean et al, 2013) explored the consequences of gamete plasticity for offspring. They (Crean et al, 2013) took advantage of the life histories of external fertilisers, dividing sperm and eggs from single individuals before conducting in vitro fertilisations, thereby excluding potentially confounding maternal effects. They (Crean et al, 2013) showed that offspring sired by sperm from males that experienced high population densities performed better in high population densities themselves, whereas offspring sired by sperm from low population density males performed better in low population densities.…”