Foundations of Gregariousness: A Dispersal Polymorphism Among the Planktonic Larvae of a Marine Invertebrate

Abstract

Theory predicts that selection should favor genotypes that can vary their tendency to disperse in habitats that are spatially or temporally variable or those that remain near their carrying capacity. Although many marine habitats appear to fit these criteria, confirmed examples of dispersal polymorphism among marine invertebrates are exceedingly rare. Competent larvae of the gregarious tubeworm, Hydroides dianthus, settle specifically in response to living conspecific worms, but a small proportion of each spawn settle nonspecifically on uninhabited substrata concurrently with their gregarious siblings. Here, using a parental half-sib analysis, we show that the proportion of a spawn settling in response to uninhabited biofilm is highly heritable. When estimated as a continuous trait based on a one-way ANOVA, heritability is estimated to be 0.83 +/- 0.31. When founder production was analyzed as a threshold trait, heritability was estimated to be 0.68 +/- 0.10 based on the breeding design experiment and 0.65 +/- 0.09 based on the artificial selection experiments. Realized heritability based on the selection experiments was considerably lower, however (0.17 per generation and 0.02 cumulative). Artificial selection was ineffectual at sequentially increasing the proportion of founder larvae among inbred family lines, but after three generations of selection, the proportion of larvae settling in response to biofilm was significantly higher among inbred lines than among the field-collected parents. The obligate planktonic larval stage common among so many marine invertebrates is thought to preclude the evolution of dispersal polymorphisms in these animals. Theoretical expectations of variable dispersal may instead be realized through individual behavioral differences resulting in differential transport or settlement preference, but this possibility remains largely unexplored among marine invertebrates.

Variation in the dispersal potential of non-feeding invertebrate larvae: the desperate larva hypothesis and larval size

“…The dispersal potential of larger larvae may be much greater than that of smaller larvae, as larger larvae can reject suboptimal settlement surfaces for longer than smaller larvae. The intraspecific differences in larval settlement behaviour and thus dispersal potential found by Toonen & Pawlik (2001a) were principally determined by genetic factors. Over 2 very different temporal scales, Jarrett (1997) and Miron et al (2000) found that energetic reserves strongly affect the settlement behaviour of barnacle cyprids (see also Harder et al 2001).…”

“…Toonen & Pawlik (1994) found that the larvae of the polychaete Hydroides dianthus also have a settlement behaviour dimorphism in which some larvae settle in response to settled conspecifics (termed 'aggregators') whilst others settle in response to unoccupied, biofilmed substratum (termed 'founders'). They further demonstrated that this settlement behaviour is heritable and argued that the behavioural dimorphism is crucial to the establishment of new populations and the maintenance of existing populations (Toonen & Pawlik 2001a). Another source of variation in larval settlement behaviour is variation in the 'desperation' of larvae.…”

“…Biologists have tended to view settling larvae as a homogenous population that reacts relatively uniformly to settlement cues (reviewed in Raimondi & Keough 1990, Toonen & Pawlik 2001a. Raimondi & Keough (1990) challenged this view and highlighted the existence of substantial intraspecific variation in the settlement behaviour of most larvae that had been studied.…”

“…Raimondi & Keough (1990) challenged this view and highlighted the existence of substantial intraspecific variation in the settlement behaviour of most larvae that had been studied. Since then, it has been suggested that this variation may be important and adaptive, particularly as a way of dealing with variation in the adult environment (Krug 2001, Toonen & Pawlik 2001a. Larval settlement behaviour also has the potential to affect larval dispersal strongly.…”

Examining the bank of microscopic stages in kelps using culturing and barcoding

“…Alternatively, the variation in recruits per sample may have been because of aggregated settlement of kelp spores. Aggregation of individuals is a pattern commonly observed in marine invertebrates (Toonen & Pawlik, 2001) and has been reported in all seaweed lineages (Dayton et al, 1984;Callow et al, 1997;Santelices et al, 2008). Because it ensures proximity of reproductive adults, and subsequently of dioecious gametophytes, gregariousness has been described as enhancing reproductive success (Maggs & Callow, 2003).…”