Reproductive patterns of deep-sea invertebrates related to phylogeny and energy availability

Abstract

Reproductive strategies and their interaction with the environment play a major role in the shaping of ecosystems. However, while our understanding of the diversity, biogeography and ecology of deep-sea invertebrates has increased considerably in the last century, little is known about the reproductive biology of most species. This is surprising, because life history strategies integrate information on the genetic, physiological and environmental factors affecting the individuals. Gametogenesis, and particularly vitellogenic pathways, are genetically determined and constrained by phylogeny. As a result, related species have similar patterns in the early processes of gamete production. In contrast, the reproductive output of an individual is strongly affected by energy availability in the environment. The number of eggs (quantified as fecundity) or their quality (size and contents of the eggs) vary with food quantity and quality and with habitat stability. Fecundity is related directly to other main life history traits, such as age at first maturity, egg size and reproductive effort, and therefore plays a major role in the life history tactics of a species. Fecundity and its relationship with environmental conditions has received special attention in this study. The hypotheses that 1)- gametogenesis is phylogenetically constrained, and 2)- fecundity and egg size are affected by food availability, were tested for several species of deep-sea invertebrates. Closely related species of caridean shrimps and asteroids from environments with different food availability were studied. Their gonad morphology, gametogenic patterns, fecundity and egg size were analysed. The reproductive biology of five species of mesopelagic shrimp from the NEAtlantic and three species of hydrothermal vent shrimp from the Mid-Atlantic Ridge was examined and compared. The gonad morphology and gametogenic processes of the eight deep-sea species were similar and characteristic of caridean shrimp. In contrast, the fecundity and egg size varied between species. In the mesopelagic shrimps, fecundity decreased and egg size increased at higher latitudes and deeper depths. These clines of fecundity and egg size are discussed in relation to environmental factors experienced by the adult females and larvae. In the hydrothermal vent shrimps, the three species produced a high number of small eggs. The fecundity of the hydrothermal vent species was significantly higher than that of the small-egged mesopelagic Acanthephyra spp. Three species of porcellanasterid asteroids from three sites (Porcupine AbyssalPlain (PAP), Madeira Abyssal Plain (MAP) and a site off NW Africa (NWA)) with differing food input were analysed. The three species had similar oogenic and spermatogenic patterns, typical of asteroid gametogenesis, at the three sites. They produced a small number of large eggs (~600 µm) in a quasi-continuous rate. The size at maturity and average adult size was significantly smaller in the specimens from the low food site (MAP). The gonad index of each species was similar at all sites, suggesting that the specimens from MAP invest relatively more energy into reproduction than growth, compared to the conspecific individuals from PAP and NWA. However, the fecundity of MAP specimens was lower than that of PAP and NWA specimens. This lower fecundity might be related to the smaller body size of adult females from MAP. The differences in energy allocation to reproduction are discussed in relation with food availability and quality.The results from this study confirm that gametogenic processes are predetermined by phylogeny in deep-sea invertebrates. In contrast, fecundity and egg size are free to fluctuate, within species-specific limits, as a response to variability in environmental factors.

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