The evolution of gonad expenditure and gonadosomatic index (GSI) in male and female broadcast‐spawning invertebrates

Abstract

Sedentary broadcast-spawning marine invertebrates, which release both eggs and sperm into the water for fertilization, are of special interest for sexual selection studies. They provide unique insight into the early stages of the evolutionary succession leading to the often-intense operation of both pre- and post-mating sexual selection in mobile gonochorists. Since they are sessile or only weakly mobile, adults can interact only to a limited extent with other adults and with their own fertilized offspring. They are consequently subject mainly to selection on gamete production and gamete success, and so high gonad expenditure is expected in both sexes. We review literature on gonadosomatic index (GSI; the proportion of body tissue devoted to gamete production) of gonochoristic broadcast spawners, which we use as a proxy for gonad expenditure. We show that such taxa most often have a high GSI that is approximately equal in both sexes. When GSI is asymmetric, female GSI usually exceeds male GSI, at least in echinoderms (the majority of species recorded). Intriguingly, though, higher male GSI also occurs in some species and appears more common than female-biased GSI in certain orders of gastropod molluscs. Our limited data also suggest that higher male GSI may be the prevalent pattern in sperm casters (where only males release gametes). We explore how selection might have shaped these patterns using game theoretic models for gonad expenditure that consider possible trade-offs with (i) somatic maintenance or (ii) growth, while also considering sperm competition, sperm limitation, and polyspermy. Our models of the trade-off between somatic tissue (which increases survival) and gonad (which increases reproductive success) predict that GSI should be equal for the two sexes when sperm competition is intense, as is probably common in broadcast spawners due to synchronous spawning in aggregations. Higher female GSI occurs under low sperm competition. Sperm limitation appears unlikely to alter these conclusions qualitatively, but can also act as a force to keep male GSI high, and close to that of females. Polyspermy can act to reduce male GSI. Higher male than female GSI is predicted to be less common (as observed in the data), but can occur when ova/ovaries are sufficiently more resource-intensive to produce than sperm/testes, for which some evidence exists. We also show that sex-specific trade-offs between gonads and growth can generate different life-history strategies for males and females, with males beginning reproduction earlier. This could lead to apparently higher male GSI in empirical studies if immature females are included in calculations of mean GSI. The existence of higher male GSI nonetheless remains somewhat problematic and requires further investigation. When sperm limitation is low, we suggest that the natural logarithm of the male/female GSI ratio may be a suitable index for sperm competition level in broadcast spawners, and that this may also be considered as an index for internally fertilizing taxa.

Releasing small ejaculates slowly increases per-gamete fertilization success in an external fertilizer: Galeolaria caespitosa (Polychaeta: Serpulidae)

“…Gametes are released into the water column by multiple individuals, polyandry is common, and sperm competition can be intense (Levitan, 1998(Levitan, , 2002(Levitan, , 2004Marshall, 2002;McEuan, 1988). Moreover, interspecific patterns of sex-specific gonadosomatic index (GSI) appear consistent with predictions from recent SCT developed for broadcast spawners (Parker et al, 2017).…”

“…Our results also suggest that interspecific patterns of sex-specific GSI in broadcast spawners should be evaluated from the perspective of natural selection in addition to sperm competition (Parker et al, 2017). For example, male-biased gonad expenditure, which remains problematic for recent SCT models for broadcast spawners (Parker et al, 2017), may reflect selection arising from high sperm wastage rather than sperm competition and sex-differences in the cost of gamete production. A crucial issue going forward is to determine the extent to which gonad expenditure in broadcast spawners is shaped by selection from the external environment during gamete dispersal vs. sperm competition.…”

“…Since the seminal work of Bateman (1948) and the development of SCT since the 1970s, observed patterns of male reproductive investment and allocation have been interpreted almost exclusively as adaptive strategies under sperm competition (Parker, 1982;Parker et al, 1972Parker et al, , 2017Wedell et al, 2002). However, broadcast spawning species have long presented a challenge to classic SCT predictions by exhibiting counter-intuitive male spawning strategies-specifically, Slow sperm release rates and weak resource-dependent allocation to ejaculates, despite massive investment in gonad tissue (Marshall & Bolton, 2007;McEuan, 1988;Olito et al, 2015;Styan & Butler, 2003).…”

“…Furthermore, broadcast spawning excludes complicating factors common in internal fertilizers such as cryptic female choice and has long been used as a model for SCT and the evolution of anisogamy (e.g. Parker, 1982;Parker, Ramm, Lehtonen, & Henshaw, 2017;Parker et al, 1972).…”

Assessing the potential for post‐ejaculatory female choice in a polyandrous beach‐spawning fish

“…Across species with limited pre‐ejaculatory sexual selection, there is generally pronounced post‐ejaculation selection (Parker et al, ). We therefore expected to find post‐ejaculation selection in the form of cryptic female choice mediated by egg cues in capelin.…”