Evolutionary transitions among dioecy, androdioecy and hermaphroditism in limnadiid clam shrimp (Branchiopoda: Spinicaudata)

Abstract

Examinations of breeding system transitions have primarily concentrated on the transition from hermaphroditism to dioecy, likely because of the preponderance of this transition within flowering plants. Fewer studies have considered the reverse transition: dioecy to hermaphroditism. A fruitful approach to studying this latter transition can be sought by studying clades in which transitions between dioecy and hermaphroditism have occurred multiple times. Freshwater crustaceans in the family Limnadiidae comprise dioecious, hermaphroditic and androdioecious (males + hermaphrodites) species, and thus this family represents an excellent model system for the assessment of the evolutionary transitions between these related breeding systems. Herein we report a phylogenetic assessment of breeding system transitions within the family using a total evidence comparative approach. We find that dioecy is the ancestral breeding system for the Limnadiidae and that a minimum of two independent transitions from dioecy to hermaphroditism occurred within this family, leading to (1) a Holarctic, all‐hermaphrodite species, Limnadia lenticularis and (2) mixtures of hermaphrodites and males in the genus Eulimnadia. Both hermaphroditic derivatives are essentially females with only a small amount of energy allocated to male function. Within Eulimnadia, we find several all‐hermaphrodite populations/species that have been independently derived at least twice from androdioecious progenitors within this genus. We discuss two adaptive (based on the notion of ‘reproductive assurance’) and one nonadaptive explanations for the derivation of all‐hermaphroditism from androdioecy. We propose that L. lenticularis likely represents an all‐hermaphrodite species that was derived from an androdioecious ancestor, much like the all‐hermaphrodite populations derived from androdioecy currently observed within the Eulimnadia. Finally, we note that the proposed hypotheses for the dioecy to hermaphroditism transition are unable to explain the derivation of a fully functional, outcrossing hermaphroditic species from a dioecious progenitor.

Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegans

“…dependent selection among demes. Also in common with Caenorhabditis, the derived self-compatible hermaphrodites of these androdioecious animals are biased in their allocation of reproductive resources towards the female function, a condition that may reflect the limited mutational options that were available to the dioecious ancestor for the evolution of self-compatibility [97,99,100].…”

Adaptive evolution of sexual systems in pedunculate barnacles

“…Phylogenetically controlled tests have identified the environmental factors responsible for the evolution of different sexual systems in other taxa, especially plants [41,51]. Few tests exist in animal taxa with diverse sexual systems comparable to those of barnacles [33], and the evolution of such systems in most cases remains to be clarified. Thus, further study is needed on the relative importance of the evolutionary forces producing the diverse sexual systems observed in animals.…”

“…They differ from normal hermaphrodites in that (i) they are always attached to specific sites of conspecifics, (ii) they allocate more resources to male function and (iii) only a few (if any) will become hermaphroditic [11,19]. In this paper, the coexistence of such dwarf males and hermaphrodites is also referred to as androdioecy, although androdioecy normally refers to the coexistence of pure males and hermaphrodites [32,33]. A species was regarded as hermaphroditic (as opposed to androdioecious) if no males were found or reported even after several non-dwarf individuals were investigated, irrespective of the sexual system of the majority of the lineage.…”

An integrative approach to species delineation incorporating different species concepts: a case study of Limnadopsis (Branchiopoda: Spinicaudata)

“…The study of Weeks et al (2009), however, hinted at the presence of even further species. To integrate their results into this study, additional analyses were carried out (Bayesian analysis and Maximum Parsimony with specifications as above; trees not shown) including all Limnadopsis individuals, as well as selected Limnadia individuals and two Eulimnadia individuals as outgroups.…”

“…Currently, eight Limnadopsis species are recognized (Richter & Timms, 2005, Timms, 2009, which all inhabit temporary water bodies in Australia. Recent molecular studies have confirmed the monophyly of Limnadopsis (Schwentner et al, 2009;Weeks et al, 2009) and have indicated the presence of further species (Weeks et al, 2009). In Spinicaudata, morphology-based taxonomy has been hampered by the extensive intraspecific plasticity of most morphological characters (e.g.…”