Improving sneaky-sex in a low oxygen environment: reproductive and physiological responses of male mosquito fish to chronic hypoxia

Abstract

SUMMARY Few studies have examined the adaptive significance of reversible acclimation responses. The aerobic performance and mating behaviour of the sexually coercive male eastern mosquito fish (Gambusia holbrooki)offers an excellent model system for testing the benefits of reversible acclimation responses to mating success. We exposed male mosquito fish to normoxic or hypoxic conditions for 4 weeks and tested their maximum sustained swimming performance and their ability to obtain coercive matings under both normoxic and hypoxic conditions. We predicted that hypoxia-acclimated males would possess greater swimming and mating performance in hypoxic conditions than normoxic-acclimated males, and vice versa when tested in normoxia. Supporting our predictions, we found the sustained swimming performance of male mosquito fish was greater in a hypoxic environment following long-term exposure to low partial pressures of oxygen. However, the benefits of acclimation responses to mating performance were dependent on whether they were tested in the presence or absence of male-male competition. In a non-competitive environment, male mosquito fish acclimated to hypoxic conditions spent a greater amount of time following females and obtained more copulations than normoxic-acclimated males when tested in low partial pressures of oxygen. When males were competed against each other for copulations, we found no influence of long-term exposure to different partial pressures of oxygen on mating behaviour. Thus, despite improvements in the aerobic capacity of male mosquito fish following long-term acclimation to hypoxic conditions, these benefits did not always manifest themselves in improved mating performance. This study represents one of the first experimental tests of the benefits of reversible acclimation responses, and indicates that the ecological significance of physiological plasticity may be more complicated than previously imagined.

Hypoxia and male behaviour in an African cichlid Pseudocrenilabrus multicolor victoriae

“…1). This supports the prediction for fewer behavioural displays in males acclimated to low DO relative to those acclimated to high DO, a pattern that is consistent with many short‐term studies that have demonstrated negative effects of hypoxia on male behavioural displays including aggressive encounters and mating displays (Sneddon & Yerbury, 2004; Abrahams et al , 2005; Marks et al , 2005; Carter & Wilson, 2006). More generally, this finding supports several reports in the literature of reduced activity levels in fishes exposed to hypoxia (Hubbs et al , 1967; Schurmann & Steffensen, 1994; Chapman & McKenzie, 2009).…”

The effects of laboratory housing and spatial enrichment on brain size and metabolic rate in the eastern mosquitofish,Gambusia holbrooki

“…The most likely explanation for this difference lies within the coercive reproductive strategy of G. holbrooki . Female mosquitofish almost never copulate willingly, and successful copulations are usually forced ( Bisazza et al, 2001 ; Carter and Wilson, 2006 ). Termed ‘sneaky sex’, males stealthily approach females and rapidly insert their gonopodium to release sperm.…”

Constraints-based stoichiometric analysis of hypoxic stress on steroidogenesis in fathead minnows, Pimephales promelas

“…Recent research has shown hypoxia to influence reproductive viability of fish by disrupting the hormonal regulation of sexual maturation and spawning (Wu et al, 2003;Dabrowski et al, 2003;Carter and Wilson, 2006;Thomas et al, 2006;Shang et al, 2006;Landry et al, 2007;Wang et al, 2008;Wu, 2009). Gene expression analyses show widespread changes in expression of genes related to erythropoiesis, angiogenesis, glycolysis (favoring anaerobic respiration), oxidative phosphorylation and steroid hormone metabolism (or steroidogenesis) (Gracey et al, 2001;Ton et al, 2003;Shang et al, 2006;Marques et al, 2008;Martinovic et al, 2009).…”