Exploring the sexual diversity of flatworms: Ecology, evolution, and the molecular biology of reproduction

Abstract

SUMMARYFlatworms exhibit huge diversity in their reproductive biology, making this group an excellent model system for exploring how differences among species in reproductive ecology are reflected in the physiological and molecular details of how reproduction is achieved. In this review, I consider five key ''lifestyle choices'' (i.e., alternative evolutionary/developmental outcomes) that collectively encompass much of flatworm sexual diversity, beginning with the decisions: (i) whether to be freeliving or parasitic; (ii) whether to reproduce asexually or sexually; and (iii) whether to be gonochoristic (separate-sexed) or hermaphroditic. I then examine two further decisions involving hermaphroditism: (iv) outcrossing versus selfing and (v) the balance of investment into the male versus the female sex function (sex allocation). Collectively, these lifestyle choices set the basic rules for how reproduction occurs, but as I emphasize in the second part of the review, the reproductive biology of flatworms is also greatly impacted by the near-pervasive and powerful pressure of sexual selection, together with the related phenomena of sperm competition and sexual conflict. Exactly how this plays out, however, is strongly affected by the particular combination of reproductive strategies adopted by each species. A striking feature of flatworms . . . is the complexity and diversity of their reproductive systems.

Self-fertilization, sex allocation and spermatogenesis kinetics in the hypodermically-inseminating flatworm Macrostomum pusillum

“…the allocation of reproductive resources into male and female reproduction (Ramm, 2017;Schärer and Ramm, 2016). Sex allocation theory investigates how an organism should partition its reproductive resources in order to gain maximal fitness in a given ecological context (Charnov, 1982).…”

“…The genus itself contains ca. 200 described species (see http://turbellaria.umaine.edu/) differing widely in various aspects of their reproduction, such as mating behaviour, sperm and genital morphology, and sex allocation (Schärer et al, 2011;Janssen et al, 2015;Ramm, 2017). Many of these traits exhibit evidence of rapid and correlated evolution, with one important distinction being the transition between those species that mate by reciprocal copulation versus those that mate by hypodermic insemination (Schärer et al, 2011), as we explain in more detail below.…”

The varied ways of being male and female

“…Ramm () provides a nice overview of the sexual diversity of flatworms, which are morphologically extremely variable and inhabit a striking range of ecological niches. A large number of quite well‐studied genetic model organisms belong to this group of animals, ranging from the free‐living planarian and Macrostomum spp.…”

“…Currently, the available data often seem to rely on only a few laboratory strains, making these sexual strategies difficult to understand in an individual versus population sex allocation context. Ramm (2016) provides a nice overview of the sexual diversity of flatworms, which are morphologically extremely variable and inhabit a striking range of ecological niches. A large number of quite well-studied genetic model organisms belong to this group of animals, ranging from the freeliving planarian and Macrostomum spp.…”

Genotype-by-environment interactions for seminal fluid expression and sperm competitive ability

“…However, the high motivation to mate more, in general, also increases the risk of receiving (excess) sperm and/or seminal fluid, and concomitantly increases risks of polyspermy, sexually transmitted pathogens and/or receipt of manipulative SFPs (Charnov, 1979; Schärer et al , 2015). Thus, it is likely that adaptations to gain control over the received ejaculate evolve in many simultaneous hermaphrodites, such as the sperm digestion common in gastropods (Baur, 1998; Michiels, 1998; Greeff & Michiels, 2017) and counter-adaptations to take control over own ejaculate such as bypassing the normal way of transferring sperm by hypodermic insemination in flatworms (Schärer et al , 2011; Ramm et al , 2015b; Ramm, 2016).…”