Patterns of self compatibility, inbreeding depression, outcrossing, and sex allocation in a marine bryozoan suggest the predominating influence of sperm competition

Abstract

Sex allocation by simultaneous hermaphrodites is theoretically influenced by selfing rate, which is in turn influenced by the benefits of enhanced genomic transmission and reproductive assurance relative to the cost of inbreeding depression. The experimental investigation of these influences in seed plants has a rich pedigree, yet although such an approach is equally relevant to colonial invertebrates, which globally dominate subtidal communities on firm substrata, such studies have been scarce. We reared self-compatible genets of the marine bryozoan Celleporella hyalina s.l. in the presence and absence of allosperm, and used molecular genetic markers for paternity analysis of progeny to test theoretical predictions that: (1) genets from focal populations with high selfing rates show less inbreeding depression than from focal populations with low selfing rates; (2) genets whose selfed progeny show inbreeding depression prefer outcross sperm (allosperm); and (3) genets bias sex allocation toward female function when reared in reproductive isolation. Offspring survivorship and paternity analysis were used to estimate levels of inbreeding depression and preference for outcrossing or selfing. Sex allocation was assessed by counting male and female zooids. As predicted, inbreeding depression was severe in selfed progeny of genets derived from the populations with low self-compatibility rates, but, with one exception, was not detected in selfed progeny of genets derived from the populations with higher self-compatibility rates. Also, as predicted, genets whose selfed progeny showed inbreeding depression preferred outcrossing, and a genet whose selfed progeny did not show inbreeding depression preferred selfing. Contrary to prediction, sex allocation in the majority of genets was not influenced by reproductive isolation. Lack of economy of male function may reflect the over-riding influence of allosperm-competition in typically dense breeding populations offering good opportunity for outcrossing. We suggest that hermaphroditism may be a plesiomorphic character of the crown group Bryozoa, prevented by phylogenetic constraint from being replaced by gonochorism and therefore not necessarily adaptive in all extant clades.

Prudent female allocation by modular hermaphrodites: female investment is promoted by the opportunity to outcross in cyclostome bryozoans

“…Restrained female allocation in the absence of allosperm should be expected only if selfing is absent or provides a lower return on reproductive investment, in fitness terms, than outcrossing. Obligate outcrossing is typical of the Celleporella hyalina clade, but the congeners C. angusta and C. osiani , which belong to a separate phylogenetic clade, freely self‐fertilize without incurring detectable inbreeding depression and show undiminished female investment in the absence of allosperm (Hughes et al ., ; Hughes & Wright, ). In contrast, Johnson () documented substantial inbreeding depression following selfing in another cheilostome bryozoan, Bugula stolonifera .…”

Sexual reproduction of the placental brooder Celleporella hyalina (Bryozoa, Cheilostomata) in the White Sea

“…C. hyalina has been an object of extensive field and experimental studies (predominantly by Hughes with co‐authors) focusing on various aspects of fertilization and sex allocation (Bishop, Manríquez, & Hughes, ; Hoare & Hughes, ; Hoare, Hughes, & Goldson, ; Hughes, Manríquez, & Bishop, ; Hughes & Wright, ; Hughes, Wright, Carvalho, & Hutchinson, ; Hughes, Wright, & Manríquez, ; Hunter & Hughes, , ; Hunter, Hughes, & Goldson, ; Manríquez, Hughes, & Bishop, , ; Pemberton, Hughes, Manríquez, & Bishop, ). Another focus has been on life‐history traits, including growth and fitness, and their plasticity (Atkinson, Morley, & Hughes, ; Cancino, ; Cancino & Hughes, , ; Eggleston, ; Hughes, , ; Hughes & Hughes, ; Hughes, Manríquez, Bishop, & Burrows, ; Hughes, Manríquez, Morley, Craig, & Bishop, ).…”

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

“…Despite the potential for self‐fertilization in bryozoans, and early studies on bryozoans even suggesting that selfing was widespread and the predominant mode of sexual reproduction (citations in Silén, ), available evidence now suggests that outcrossing is common in bryozoans (Hoare & Hughes, ; Hunter & Hughes, ; Ryland & Bishop, ; Silén, ; Temkin, ; Yund & McCartney, ). It should also be noted, however, that the self‐fertilization rate does vary considerably within some species and negatively covaries with inbreeding depression (Hughes et al, ). In Bugula stolonifera , fertilization success per colony in colonies reared in isolation ranged from 38% and 59% (Johnson, ).…”

“…Few studies have investigated cues for sperm release in bryozoans, but sperm release has been induced by light in some species (e.g., Celleporella hyalina ) (Manríquez, Hughes, & Bishop, ). Furthermore, in C. hyalina , investment in male zooids depends on environmental conditions (Hunter & Hughes, ), rather than conspecific cues (Hughes et al, ), though colonies produce more male zooids at colony edges that contact a physical barrier, including the edge of the same or different colony (Hoare et al, ).…”

“…The fitness effects of biparental inbreeding in animals with separate sexes are also expected to be sex‐specific (Parker, ; Szulkin et al, ; Waser, Austad, & Keane, ), but sex‐specific effects of self‐fertilization and biparental inbreeding in hermaphrodites have received much less attention (though see, for example, Carr & Dudash, ; Hughes, Wright, Carvalho, & Hutchinson, ; Janicke, Vellnow, Sarda, & David, ; Rausher & Chang, ; Willis, ). Nonetheless, sex‐specific effects of inbreeding in hermaphrodites are also possible and, like in gonochoristic animals, have potential to create sexually antagonistic selection over whether to avoid or prefer inbreeding (Kokko & Ots, ; Parker, ).…”