Experimental evidence for reduced male allocation under selfing in a simultaneously hermaphroditic animal

Abstract

Self-fertilization is widespread among simultaneously hermaphroditic animals and plants, but is often only facultatively deployed under circumstances that constrain outcrossing. A central prediction of sex allocation (SA) theory is that because exclusive selfing reduces sperm or pollen competition to zero, this should favour extreme economy in resources channelled to the male sex function. We can therefore expect that organisms switching from outcrossing to selfing should reduce their male allocation. However, to date this prediction has received relatively little support in animal taxa, especially compared to plants. Here we show that isolated individuals (under enforced selfing conditions) have a less male-biased SA than do grouped conspecifics (under outcrossing conditions) in the preferentially outcrossing flatworm Macrostomum hystrix. This shift arises from a reduced male allocation (testis area) in isolated individuals, although we did not find any evidence for a re-allocation of these resources to the female sex function (i.e. ovary area was unaffected by selfing/outcrossing conditions). Our results provide some of the clearest experimental evidence to date for reduced male allocation under selfing in simultaneously hermaphroditic animals, extending previous findings comparing SA between populations differing in selfing rates to the level of individual plasticity in gametogenesis.

Variation in sex allocation plasticity in three closely related flatworm species

“…Interestingly, an earlier study in M. pusillum —a species that regularly self‐fertilizes—has shown that the species does not exhibit any plasticity in SA in response to group size (Giannakara & Ramm, ). In contrast, M. hystrix —a facultatively self‐fertilizing species—does adjust its SA depending on group size (Winkler & Ramm, ). This suggests that the degree of self‐fertilization could also influence sperm competition and therefore SA and its plasticity.…”

“…While SA plasticity in response to mating group size is widespread in hermaphroditic animals (reviewed in Schärer, ), the strength and nature of the plasticity vary both among and within species, with some studies showing plasticity only in the male function (Baeza, ; Hoch & Levinton, ; Janicke et al, ; Schärer & Janicke, ; Schärer & Ladurner, ; Winkler & Ramm, ) or the female function (Lorenzi et al, ; Schleicherová et al, ), while other studies show plasticity in either both functions (Janicke & Schärer, , ) or no plasticity at all (Giannakara & Ramm, ). Although a part of this variation in these estimates of plasticity may reflect biases due to the ease with which male and female allocation can be measured in different study systems, it might also reflect different reproductive modes (with different postcopulatory processes, Schärer & Pen, ), species‐specific costs of plasticity (Schleicherová et al, ), or different evolutionary histories (Schleicherová, Sella, & Lorenzi, ).…”

“…The free-living flatworm genus Macrostomum is an excellent model system for studying variation in SA plasticity, since reproductive organs can be measured accurately, repeatedly, and noninvasively in multiple species in the genus (e.g., Giannakara & Ramm, 2017;Schärer & Ladurner, 2003;Winkler & Ramm, 2018), allowing us to quantify and compare SA across closely related species. Earlier studies on the model organism Macrostomum lignano have shown that it has plastic SA, with SA increasing (i.e., becoming more malebiased) with increasing group size (e.g., Schärer & Ladurner, 2003).…”

Is the initiation of selfing linked to a hermaphrodite’s female or male reproductive function?

“…Under these conditions, the generation time is approximately 25 days (Ramm et al 2012). The culture maintained in the laboratory is an inbred line, called SR1 (Zadesenets et al 2016;Winkler and Ramm 2018), which was started in 2011 based on an outbred M. hystrix culture, which initially derived from worms collected in May 2010 from the San Rossore Regional Park (43.684°N…”

Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

“…In Macrostomum, traumatic insemination is called hypodermic insemination, since in several species the donor uses a needle-like stylet (Fig 1) to inject sperm through the epidermis of the mating partner and sperm then move through the body of the recipient to the site of fertilisation [41,57,58]. Injected sperm can often be observed inside the parenchymal tissues of these highly transparent animals [41,[57][58][59], making it feasible to screen a large number of species for the convergent evolution of hypodermic insemination. And while we here present evidence that not all traumatically mating Macrostomum species may inject sperm through the external epidermis, we nevertheless use the term hypodermic insemination for consistency with the earlier literature.…”