Transgenerational plasticity for sexual reproduction and diapause in the life cycle of monogonont rotifers: intraclonal, intraspecific and interspecific variation in the response to crowding

Abstract

Summary 1.In monogonont rotifers parthenogenetic reproduction allows population growth, and mictic (sexual) reproduction leads to the production of diapausing eggs. When amictic females are exposed to a mixis stimulus, they produce mictic daughters, whose eggs develop into males or, if fertilized, into diapausing eggs. Experiments showed that mictic offspring production is initiated by crowding in females of angularis , E. senta and R. frontalis , the propensity of amictic females to respond to crowding by producing mictic female offspring is low in the stem female hatching from a diapausing egg, but then increases after some generations. In many cases, only few mictic offspring are produced by crowded females of the second to the fifth generation, but the maximal response occurs only in later generations. Delayed sexual reproduction in early generations from the resting egg may be advantageous, because it first favours rapid population growth and later on maximizes resting egg production. However, it may be disadvantageous, if unpredictable environmental variation causes a population decline when sexual reproduction is still suppressed. 3. The extent to which sexual reproduction is delayed varies among and within species. When strains from populations in temporary and permanent habitats were compared, sexual reproduction was significantly delayed in strains from temporary habitats in all species, whereas in B. calyciflorus and R. frontalis mixis was not significantly delayed in strains from permanent habitats. In E. senta mixis was significantly delayed in clones from both habitat types. 4. Within all strains there was significant variation among clones in the propensity to produce mictic offspring, the extent to which sexual reproduction was delayed in the first generations after the stem female hatched, or both.

Specificity of the crowding response in the Brachionus plicatilis species complex

“…Although Gilbert provided stimuli large enough to induce mixis, these females continued to reproduce asexually, and only after several generations responded to the mixis stimulus. This transgenerational effect has been demonstrated in other rotifer species as well (Schroder and Gilbert 2004), although it has yet to be tested in B. plicatilis. Nevertheless, if delayed mixis exists in B. plicatilis, it could provide a mechanism to prevent a low-abundance species having just emerged from resting eggs from being induced by a highly abundant co-occurring species.…”

Modes, mechanisms and evidence of bet hedging in rotifer diapause traits

“…This study reaches up to Category II a , as it does not hold an among-population comparison. Additionally, several other empirical studies have reported variability in the timing of sex among rotifer populations of different species and from different habitats (Category II b ; Schröder & Gilbert, 2004;Gabaldón & Carmona, 2015), but they fail to look at the match between this variability and the degree of environmental unpredictability. We conclude that evidence for bet hedging in the timing of sex is still weak, likely because of several reasons: (1) many studies often lack accurate measurements for habitat predictability-due to the fact that appropriate metrics for the organism on focus and long-term monitoring are required (García-Roger et al 2014), (2) confounding effects such as the possible relationship between growing season length and predictability are not dissected (e.g.…”

“…The timing of sex has been proposed as an instance of the conservative bet-hedging trait in rotifer populations inhabiting unpredictable environments (Carmona et al, 1995;Serra & King, 1999;Schröder & Gilbert, 2004;Serra et al, 2004;Gilbert, 2007a). If the end of the growing season-or the nutritional conditions required for diapausing egg production (Gilbert, 2010)-cannot be predicted by rotifers, then producing diapausing eggs as soon as possible can avoid the risk of a zero-fitness event.…”

“…Carmona et al, 1994Carmona et al, , 1995Snell & Boyer, 1988;Gilbert, 2002;Schröder & Gilbert, 2004;Gilbert & Schröder, 2007;Carmona et al, 2009). However, despite this variability, the sexual reproduction ratio is almost never 100%, and commonly, it is not higher than 30%; thus, some fraction of the population continues reproducing asexually when sexual reproduction is initiated (Gilbert, 1974;Pourriot & Clément, 1975;Carmona et al, 1995;Schröder, 2001;Gilbert, 2002;Schröder, 2005).…”

“…After revisiting the existing rotifer literature, we found that bet hedging has been proposed to evolve in at least three diapause-related traits: (1) the timing of sex, which in practice is used as a proxy of the timing of diapausing egg production and typically measured as the population density threshold for sexual reproduction initiation (i.e. the lowest the threshold, the earliest the timing of sex; Carmona et al, 1995;Schröder & Gilbert, 2004;Serra et al, 2004;Schröder, 2005;Carmona et al, 2011); (2) the sexual reproduction ratio (best known as the mixis ratio and computed as the fraction of sexually reproducing females in the population) (Gilbert, 2003;Fussmann et al, 2007;Gilbert & Schröder, 2007) and (3) the timing of diapausing egg hatching (i.e. the fraction of diapausing eggs hatching at the beginning of a new growing season) (Schröder, 2005;García-Roger et al, 2014).…”