Density drives polyandry and relatedness influences paternal success in the Pacific gooseneck barnacle, Pollicipes elegans

Abstract

BackgroundPolyandry is a common mating strategy in animals, increasing female fitness through direct (material) and indirect (genetic) benefits. Most theories about the benefits of polyandry come from studies of terrestrial animals, which have relatively complex mating systems and behaviors; less is known about the potential benefits of polyandry in sessile marine animals, for which potential mates may be scarce and females have less control over pre-copulatory mate choice. Here, we used microsatellite markers to examine multiple paternity in natural aggregations of the Pacific gooseneck barnacle Pollicipes elegans, testing the effect of density on paternity and mate relatedness on male reproductive success.ResultsWe found that multiple paternity was very common (79% of broods), with up to five fathers contributing to a brood, though power was relatively low to detect more than four fathers. Density had a significant and positive linear effect on the number of fathers siring a brood, though this relationship leveled off at high numbers of fathers, which may reflect a lack of power and/or an upper limit to polyandry in this species. Significant skew in male reproductive contribution in multiply-sired broods was observed and we found a positive and significant relationship between the proportion of offspring sired and the genetic similarity between mates, suggesting that genetic compatibility may influence reproductive success in this species.ConclusionsTo our knowledge, this is the first study to show high levels of multiple paternity in a barnacle, and overall, patterns of paternity in P. elegans appear to be driven primarily by mate availability. Evidence of paternity bias for males with higher relatedness suggests some form of post-copulatory sexual selection is taking place, but more work is needed to determine whether it operates during or post-fertilization. Overall, our results suggest that while polyandry in P. elegans is driven by mate availability, it may also provide a mechanism for females to ensure fertilization by compatible gametes and increase reproductive success in this sessile species.

Higher reproductive success for chimeras than solitary individuals in the kelp Lessonia spicata but no benefit for individual genotypes

“…more genotypes contributing to the passing of alleles through generations than expected from the number of macroscopic units identified by the holdfast. In addition, chimerism may play an important role in promoting outcrossing, as observed in aggregations of the barnacle Pollicipes elegans (Plough et al 2014). This may be particularly relevant if selfing brings costs due to inbreeding depression, as suggested for the giant kelp M. pyrifera (Johansson et al 2013).…”

Cryptic Female Choice in Crustaceans

“…8.1). In contrast, males of higher genetic similarity Shuster (1989aShuster ( , b, 1990 to the female achieved higher offspring ratios in the Pacific gooseneck barnacle (Pollicipes elegans)-this has been speculated to reflect improved gametic recognition during fertilization, the function and benefit of which will have to be resolved in future studies (Plough et al 2014) (Fig. 8.1).…”

“…In crustaceans, spermcast mating has recently been reported for barnacles, which usually employ their penis for sperm transfer (Barazandeh et al 2013). The high level of multiple paternity in some barnacle species and the fact that genetically related fathers sire more offspring (Plough et al 2014) are intriguing observations, suggesting that similar choice mechanisms as reported for other spermcasting taxa might be at play.…”

“…a In the shrimp Caridina ensifera, paternity is in favor of genetically dissimilar males (genetic similarity index after Nei and Li 1979;Yue and Chang 2010). b In contrast, the barnacle Pollicipes elegans shows biased paternity in favor of genetically similar males (genetic similarity index after Li et al 1993;Plough et al 2014) events such as oviposition, copulation, or receptivity, which may increase encounter probability with favored males. Intensified male-male competition can be provoked through female chemical signaling mediated by sex pheromones (Berry and Breithaupt 2010;Okamura and Goshima 2010), which may also elicit male search and guarding behavior (Yano et al 1988;Bouchard et al 1996;Sneddon et al 2003).…”

High levels of polyandry, but limited evidence for multiple paternity, in wild populations of the western rock lobster (Panulirus cygnus)

“…For the most part, however, parentage studies on decapods have been conducted on crabs (Baggio et al., ; Jensen & Bentzen, ; Jossart et al., ; Koga, Henmi, & Murai, ; McKeown & Shaw, ; Pardo, Riveros, Fuentes, Rojas‐Hernandez, & Veliz, ; Reaney, Maurer, Backwell, & Linde, ; Sainte‐Marie, Gosselin, Sevigny, & Urbani, ). In some cases, where multiple paternity has been detected, considerable skews in fertilization success toward a single male have been reported (Bailie et al., , ; Gosselin, Sainte‐Marie, & Bernatchez, ; Plough, Moran, & Marko, ). Such skew may result from a range of postmating processes, including cryptic female choice (Thiel & Hinojosa, ) and sperm competition (Diesel, ; Sévigny & Sainte‐Marie, ; Urbani, Sainte‐Marie, Sévigny, Zadworny, & Kuhnlein, ).…”