Prior selfing and the selfing syndrome in animals: an experimental approach in the freshwater snailBiomphalaria pfeifferi

Abstract

SummaryInbreeding species of hermaphroditic animals practising copulation have been characterized by few copulations, no waiting time (the time that an isolated individual waits for a partner before initiating reproduction compared with paired individuals) and limited inbreeding (self-fertilization) depression. This syndrome, which has never been fully studied before in any species, is analysed here in the highly selfing freshwater snail Biomphalaria pfeifferi. We conducted an experiment under laboratory conditions over two generations (G 1 and G 2 ) using snails sampled from two populations (100 individuals per population). G 1 individuals were either isolated or paired once a week (potentially allowing for crosses), and monitored during 29 weeks for growth, fecundity and survival. Very few copulations were observed in paired snails, and there was a positive correlation in copulatory activity (e.g. number of copulations) between the male and female sexual roles. The waiting time was either null or negative, meaning that isolated individuals initiated reproduction before paired ones. G 2 offspring did not differ in hatching rate and survival (to 28 days) between treatments, but offspring from paired individuals grew faster than those from isolated individuals. On the whole, the self-fertilization depression was extremely low in both populations. Another important result is that paired G 1 individuals began laying (selfed) eggs several weeks prior to initiating copulation : this is the first characterization of prior selfing (selfing initiated prior to any outcrossing) in a hermaphroditic animal. A significant population effect was observed on most traits studied. Our results are discussed with regard to the maintenance of low outcrossing rates in highly inbreeding species.

Does life in unstable environments favour facultative selfing? A case study in the freshwater snail Drepanotrema depressissimum (Basommatophora: Planorbidae)

“…Individuals from predominantly selfing species are much more reluctant to copulate in similar conditions. For example, Tian-Bi et al (2008) observed one copulation every (about) ten observation sessions in two populations of Biomphalaria pfeifferi. It therefore seems that monitoring the mating behaviour of sexually mature individuals, which have been isolated for a long enough time, is a simple and informative way to characterize the dominant mating system, at least in freshwater snails (Doums et al 1996;Escobar et al 2011).…”

“…Escobar et al (2011) have compiled data on 22 pulmonate species (plus 3 other hermaphroditic animals) and concluded that most species fall into three ''syndromes'': the first combined very high or total inbreeding depression, no selfing in natural populations, and very long waiting times (type A in Table 1); the second associated moderate inbreeding depression, rare selfing in the wild, and moderate waiting times (type B); and the third was characterized by very little inbreeding depression, high selfing rates and no waiting time (type D). Copulation frequency has also been suggested to correlate with the outcrossing rate (Doums et al 1996, Tian-Bi et al 2008. However very few studies simultaneously report behavioural traits (copulation frequency), life-history traits (waiting time), estimates of inbreeding depression and robust estimates of selfing rates.…”

Complex heterochrony underlies the evolution ofCaenorhabditis eleganshermaphrodite sex allocation

“…Some of these ideas have been experimentally examined by manipulating mating or cross‐pollination opportunities (Tian‐Bi et al. ; Dorken and Pannell ; Roels and Kelly ), the level of resources available for reproduction and survival (Mazer et al. ; Case and Ashman ), and by manipulating the reproductive system (Teotonio et al.…”

“…; Tian‐Bi et al. ; Escobar et al. ) and, in the case of angiosperms, with differential timings and rates of germline and somatic tissue development within flowers (Darwin ; Harder and Barrett ; Li and Johnston ; Geuten and Coenen ).…”

“…Some of these ideas have been experimentally examined by manipulating mating or cross-pollination opportunities (Tian-Bi et al 2008;Dorken and Pannell 2009;Roels and Kelly 2011), the level of resources available for reproduction and survival (Mazer et al 2003;Case and Ashman 2007), and by manipulating the reproductive system (Teotonio et al 2012;Carvalho et al 2014b;Theologidis et al 2014). Despite these studies, however, it remains mostly unknown which developmental changes underlie the evolution of hermaphrodite sex allocation under selfing and/or outcrossing (Li and Johnston 2010;Roels and Kelly 2011;Noel et al 2016).…”