RESEARCH ARTICLE Cherchez la femme – impact of ocean acidification on the egg jelly coat and attractants for sperm Shawna A. Foo 1, *, Dione Deaker 2 and Maria Byrne 3 ABSTRACT The impact of ocean acidification on marine invertebrate eggs and its consequences for sperm chemotaxis are unknown. In the sea urchins Heliocidaris tuberculata and Heliocidaris erythrogramma, with small (93 μm) and large (393 μm) eggs, respectively, we documented the effect of decreased pH on the egg jelly coat, an extracellular matrix that increases target size for sperm and contains sperm-attracting molecules. In near-future conditions (pH 7.8, 7.6), the jelly coat of H. tuberculata decreased by 11% and 21%, reducing egg target size by 9% and 17%, respectively. In contrast, the egg jelly coat of H. erythrogramma was not affected. The reduction in the jelly coat has implications for sperm chemotaxis in H. tuberculata. In the presence of decreased pH and egg chemicals, the sperm of this species increased their velocity, motility and linearity, behaviour that was opposite to that seen for sperm exposed to egg chemicals in ambient conditions. Egg chemistry appears to cause a reduction in sperm velocity where attractants guide the sperm in the direction of the egg. Investigation of the effects of decreased pH on sperm isolated from the influence of egg chemistry does not provide an integrative assessment of the effects of ocean acidification on sperm function. Differences in the sensitivity of the jelly coat of the two species is likely associated with egg evolution in H. erythrogramma. We highlight important unappreciated impacts of ocean acidification on marine gamete functionality, and insights into potential winners and losers in a changing ocean, pointing to the advantage conveyed by the evolution of large eggs. KEY WORDS: Egg extracellular matrix, Egg size, Target size, Broadcast spawning, Sperm chemotaxis, Heliocidaris INTRODUCTION As the ocean is on a trajectory of increased acidification because of increased uptake of atmospheric CO 2 (IPCC, 2014), there are major concerns for the functionality of the gametes of free-spawning species. These cells are fundamental for the propagation and persistence of marine populations that are directly exposed to environmental conditions (Pechenik, 1987), where surface ocean pH is projected to drop by 0.3 pH units by 2100 (IPCC, 2014). Thus far, investigation of the impacts of ocean acidification (OA) on sperm physiology and motility has been conducted with sperm isolated from the influence of egg chemistry (reviewed in Campbell et al., 2016). The impact of OA on the egg cell and its consequences for egg chemistry and sperm chemotaxis are unknown (Foo and Byrne, 2017). The eggs of many marine invertebrates are surrounded by a jelly coat, including those of echinoderms, many molluscs and some polychaetes (Suzuki, 1989; Rosati, 1995; Farley and Levitan, 2001; Podolsky, 2002; Hofmann, 2013; Plickert, 2013). In sea urchins, the jelly coat is a polysaccharide–glycoprotein extracellular matrix that hydrates in contact with seawater and is known to be sensitive to low pH (Podolsky, 2002; Dale and de Felice, 2011; Vacquier, 2011), and so may be vulnerable to OA. In molluscs and polychaetes, the egg jelly coat can be quite diffuse (Anderson and Eckberg, 1983; Focarelli et al., 1991), and thus most studies of the chemical nature and function of the egg jelly coat have focused on echinoderms. In echinoderms, the jelly coat serves many roles before and during fertilisation. Jelly coats provide mechanical support for the egg, reducing the shear stress that eggs experience when passing through the gonopore (Thomas and Bolton, 1999; Bolton et al., 2000). The jelly coat is an economical way to increase egg target size for sperm, thereby facilitating fertilisation success (Vogel et al., 1982; Farley and Levitan, 2001; Podolsky, 2002). The sialic acid and glycan content of the egg jelly coat shows interspecific and intraspecific differences in sea urchins, and this influences differences in the hydration of egg jelly after spawning (Jondeung and Czihak, 1982; Pomin, 2015). The effect of removal of the egg jelly coat on fertilisation is not well understood, with conflicting results. Studies that report little or no effects of jelly coat removal are largely short-term experiments involving high levels of sperm and where removal of the jelly coat increased fertilisation rate by removal of a barrier (Hagström, 1959; Vacquier et al., 1978). In contrast, studies investigating fertilisation in sperm-limiting conditions show that removal of the egg jelly coat decreased fertilisation success (McLaughlin and Humphries, 1978; Styan, 1998). For Lytechinus variegatus, eggs with intact jelly coats accrued 2.2 more collisions with sperm compared with eggs without jelly coats, which required double the amount of sperm to achieve 50% fertilisation (Farley and Levitan, 2001). Several studies of echinoids, asteroids and abalone have shown that the jelly coat possesses chemoattractive properties (Miller, 1985; Suphamungmee et al., 2010; Riffell et al., 2002). The egg jelly coat of sea urchins contains the short peptides speract and resact, which attract sperm, stimulate sperm metabolism and influence the orientation of the sperm, thereby increasing the probability of fertilisation (Miller, 1985; Matsumoto et al., 2003; Islam et al., 2008). Compounds in the jelly coat have been shown to promote directional swimming and altered swimming paths in sperm to maximise fertilisation success (Fitzpatrick et al., 2012; Jikeli et al., 2015). These compounds also stimulate the acrosome reaction to promote conspecific sperm–egg binding (Matsui et al., 1986). For the mussel Mytlius galloprovincialis, egg molecules act as a selective barrier to promote fertilisation by more compatible sperm, with the most successful male ejaculate having the lowest percentage of motile sperm (Fitzpatrick et al., 2012). Received 8 January 2018; Accepted 16 April 2018 1 Department of Global Ecology, Carnegie Institution for Science, Stanford, CA 94305, USA. 2 Department of Anatomy and Histology, School of Medical Sciences, The University of Sydney, Sydney, NSW 2006, Australia. 3 Department of Anatomy and Histology, School of Medical Sciences, and School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW 2006, Australia. *Author for correspondence (sfoo@carnegiescience.edu) S.A.F., 0000-0002-7083-2377 1 © 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb177188. doi:10.1242/jeb.177188 Journal of Experimental Biology