Reproductive Plasticity in Freshwater Invader: From Long-Term Sperm Storage to Parthenogenesis

Abstract

Orconectes limosus, a North American crayfish species, is one of the most important aquatic invaders in European inland waters. Despite more than 120 years occurrence in Europe and intense research, there are still gaps in knowledge of its life history and ecology. Investigation into O. limosus invasive success requires identifying the mechanisms that enabled them to establish dense and widespread populations from small initial numbers without observable limitation by an introduction bottleneck. In part, O. limosus success may lie in its ability to reproduce by facultative parthenogenesis. Moreover, there are possible other mating scenarios, because of two mating seasons (autumn and spring) in O. limosus. This work investigated the effect of four reproductive scenarios (autumn mating only, spring mating only, autumn and spring mating, and without mating) on the reproductive success of O. limosus. Females successfully reproduced in all tested mating regimes using parthenogenesis as well as log term sperm storage. This reproductive plasticity likely facilitates the overwhelming success of O. limosus spread and establishment in new localities. It can explain the spread of O. limosus from the initial introduction of 90 specimens to most of continental Europe and Great Britain. These conclusions imply a serious threat, not only for autochthonous European astacofauna, but for other aquatic organisms as well as entire ecosystems.

Evidence for multiple paternity in two species of Orconectes crayfish

“…Observations of multiple mating attempts of female crayfish by two or more male crayfish have been made in captivity (Berrill and Arsenault 1982;Reynolds 2002;Buřič et al 2013), and many laboratory studies have addressed the reproductive ecology of crayfish (e.g., Snedden 1990;Rubolini et al 2007;Gherardi 2008a, 2008b;Galeotti et al 2009). However, few studies have examined genetic paternity; here, we infer that females not only copulate with multiple males, but that they use the sperm from more than one male to fertilize their eggs.…”

“…Crustacean decapods have nonmotile sperm encapsulated in single or multiple spermatophores that are transferred to the female externally or internally (Reynolds 2002), enabling manipulation of fertilization by males and females. In crayfish, females produce usually a single brood annually and have the capacity to store sperm in their spermatheca throughout a mating season (Holdich and Reeve 1988;Buřič et al 2013), permitting multiple paternity within a single brood when the female is polyandrous and sperm mixing occurs. Male crayfish may bias paternity in their favor via several mating behaviors such as extruding sperm plugs (Holdich and Reeve 1988), interrupting mating pairs (Stein 1976), diluting sperm masses , and removing sperm masses from previous males (Villanelli and Gherardi 1998;Galeotti et al 2007).…”

Fate of glair glands and spawning behaviour in unmated crayfish: a comparison between gonochoristic slough crayfish and parthenogenetic marbled crayfish

“…In unmated females of laboratory-raised Cherax destructor (Parastacidae) the spawning behaviour was quite diverse: about 20% spawned when raised at 30°C but none at 27°C (Tropea et al 2010). Spawning of unmated females also occurred in facultatively parthenogenetic females of the cambarid Orconectes limosus (Buřič et al 2011(Buřič et al , 2013. Out of 30 unmated parthenogenetic females 28 spawned and only one female did not spawn (the remaining individual died) (Buřič et al 2011), resembling the situation in marbled crayfish.…”

Different aspects of reproduction strategies in crayfish: A review

“…However, the possibility exists that this reproduction behaviour mode is more widespread among cambarids, and may contribute to the success of this group when colonizing new habitats and territories. Asexual generations may also have contributed to observations of supposed P. clarkii clones by Yue et al (2008), and possibly to significant heterozygote deficiencies observed in Chinese populations of P. clarkii (Yue et al, 2010) as well as in some recent studies of existing invasive populations of O. limosus in the Czech Republic (Filipova et al, 2009), up to now explained by founder effects or assortative mating (Buřič et al, 2011(Buřič et al, , 2013.…”

“…The time period between copulation and ovulation varies, ranging from days to weeks (Vogt, 2002) or even several months (Buřič et al, 2013). A dense secretion is released from glair glands that dissolves spermatophore wall and releases spermatozoa across the abdominal part of the female body.…”