Variation in sex allocation plasticity in three closely related flatworm species

Ballmer

Laubscher

et al. 2020

Sci Rep

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Reproductive traits are some of the fastest diverging characters and can serve as reproductive barriers. The free-living flatworm Macrostomum lignano , and its congener M. janickei are closely related, but differ substantially in their male intromittent organ (stylet) morphology. Here, we examine whether these morphological differences are accompanied by differences in behavioural traits, and whether these could represent barriers to successful mating and hybridization between the two species. Our data shows that the two species differ in many aspects of their mating behaviour. Despite these differences, the species mate readily with each other in heterospecific pairings. Although both species have similar fecundity in conspecific pairings, the heterospecific pairings revealed clear postmating barriers, as few heterospecific pairings produced F1 hybrids. These hybrids had a stylet morphology that was intermediate between that of the parental species, and they were fertile. Finally, using a mate choice experiment, we show that the nearly two-fold higher mating rate of M. lignano caused it to mate more with conspecifics, leading to assortative mating, while M. janickei ended up mating more with heterospecifics. Thus, while the two species can hybridize, the mating rate differences could possibly lead to higher fitness costs for M. janickei compared to M. lignano .

Section: Methodsmentioning

confidence: 99%

Successful mating and hybridisation in two closely related flatworm species despite significant differences in reproductive morphology and behaviour

Ballmer

Laubscher

et al. 2020

Sci Rep

Self Cite

“…The journal's Online ISSN is 1439‐0469 and it is archived in CLOCKSS. Note that these names have also appeared in the electronic 'Early View' edition of another article from our group (Singh, Vellnow, & Schärer, ), but since that work was not intended to conform to the ICZN requirements, having an experimental rather than taxonomic focus, these names cannot be considered available from that work.…”

Section: Methodsmentioning

confidence: 99%

A phylogenetically informed search for an alternative Macrostomum model species, with notes on taxonomy, mating behavior, karyology, and genome size

Schärer

Brand

et al. 2019

J Zool Syst Evol Res

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The free‐living flatworm Macrostomum lignano is used as a model in a range of research fields—including aging, bioadhesion, stem cells, and sexual selection—culminating in the establishment of genome assemblies and transgenics. However, the Macrostomum community has run into a roadblock following the discovery of an unusual genome organization in M. lignano, which could now impair the development of additional resources and tools. Briefly, M. lignano has undergone a whole‐genome duplication, followed by rediploidization into a 2n = 8 karyotype (distinct from the canonical 2n = 6 karyotype in the genus). Although this karyotype appears visually diploid, it is in fact a hidden tetraploid (with rarer 2n = 9 and 2n = 10 individuals being pentaploid and hexaploid, respectively). Here, we report on a phylogenetically informed search for close relatives of M. lignano, aimed at uncovering alternative Macrostomum models with the canonical karyotype and a simple genome organization. We taxonomically describe three new species: the first, Macrostomum janickei n. sp., is the closest known relative of M. lignano and shares its derived genome organization; the second, Macrostomum mirumnovem n. sp., has an even more unusual genome organization, with a highly variable karyotype based on a 2n = 9 base pattern; and the third, Macrostomum cliftonensis n. sp., does not only show the canonical 2n = 6 karyotype, but also performs well under standard laboratory culture conditions and fulfills many other requirements. M. cliftonensis is a viable candidate for replacing M. lignano as the primary Macrostomum model, being outcrossing and having an estimated haploid genome size of only 231 Mbp.

“…22, with the SA data reported in, respectively, Giannakara and Ramm (2017), Winkler and Ramm (2018), and Supplementary Information S1. An additional four species are reciprocally mating, namely M. janickei Schärer, 2019, M. cliftonense Schärer and Brand, 2019, and M. mirumnovem Schärer and Brand, 2019(Schärer et al 2020Zhang et al 2021), with the SA data reported in Singh et al (2020b), plus multiple studies in M. lignano Ladurner, Schärer, Salvenmoser, andRieger, 2005 (Ladurner et al 2005), with the SA data reported in several studies (see below). Details of all the SA studies are given in Supplementary Table S1.…”

Section: Study Speciesmentioning

confidence: 99%

“…The species M. mirumnovem (Singh et al 2020b) and all three hypodermically inseminating species (Ramm et al 2012(Ramm et al , 2015Giannakara and Ramm 2017, this study) can self-fertilize, and were classified accordingly. Moreover, we classified species as either reciprocally mating or hypodermically inseminating using both behavioural and morphological data.…”

Section: Study Speciesmentioning

confidence: 99%

“…Moreover, both reciprocally mating and hypodermically inseminating species possess a female antrum, but in the latter this organ has a simple morphology and presumably serves only for egg-laying, while in the former it is usually more complex and used both for egg-laying and for receiving sperm from the partner (Schärer et al 2011;Brand et al 2021a). Interestingly, hypodermic insemination is also associated with a suite of morphological traits that potentially facilitate self-fertilization (Ramm et al 2012(Ramm et al , 2015Giannakara and Ramm 2017), although self-fertilization has recently also been documented in at least one reciprocally mating species, M. mirumnovem (Singh et al 2020b).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Self-fertilization, but not mating strategy, predicts the evolution of sex allocation plasticity in a hermaphroditic flatworm genus

Schärer

2020

Preprint

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Local sperm competition (LSC), which occurs when related sperm compete for access to a given set of eggs, can influence sex allocation (SA) in simultaneous hermaphrodites. Different factors that have been predicted to affect LSC—and hence, optimal SA—include the mating strategy (such as reciprocal mating vs. hypodermic insemination) and the ability to self-fertilize. Moreover, the level of LSC experienced could vary temporally and/or spatially, favouring the evolution of SA plasticity. However, it is unknown how the mating strategy and ability to self-fertilize can influence SA and SA plasticity. Here, we explored this by collecting estimates of SA and SA plasticity for seven species of the flatworm genus, Macrostomum, and performing analyses while controlling for phylogeny. While we found substantial interspecific variation in SA, neither the mating strategy nor the ability to self-fertilize had a significant effect on SA. Next, we estimated standardized effect sizes for SA plasticity in response to i) the presence of mating partners and ii) the strength of LSC for each species, and tested if the mating strategy or ability to self-fertilize predicted these effect sizes. We found considerable interspecific variation in SA plasticity, with some species being highly plastic and others showing no significant plasticity. Moreover, self-fertilization predicted SA plasticity with respect to the presence of mating partners, with SA plasticity being lower for self-fertilizing species. Finally, we showed that interspecific variation in SA is nearly three times higher than intraspecific variation, suggesting that SA estimates in field-collected specimens can, at least to some degree, be interpreted as representing interspecific rather than intraspecific variation. Our study suggests that both SA and SA plasticity can evolve rapidly, with self-fertilization being an important predictor for the latter in Macrostomum.