Week 05: Simultaneous Hermaphroditism

As an evolutionary biologist and an invertebrate zoologist, I’ve long been interested in the diversity of mating systems that are found in animals (and plants!). In particular, I’m interested in the co-occurrence of male and female traits in a single individual. How does having both male and female traits influence who you mate with and how you take care of your offspring?? These characteristics are found in plants and animals that produce both eggs (or seeds) and sperm (or pollen) at the same time (simultaneously!). We call these organisms simultaneous hermaphrodites.

We find examples of simultaneous hermaphroditism in many different plants and animals across their respective kingdoms including many that you are likely already familiar with: earthworms, leaches, snails, slugs, sponges, barnacles, and most flowering plants, to name a few.

Fascinating behaviors often accompany the ability to make both sperm and eggs at the same time. In certain flatworms, each individual has a penis armed with a needle sharp stylet. When mating in initiated, a pair of flatworms battle it out to inject their rival with sperm.

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Figure 1: Flatworm ‘penis fencing’ (Image credit)

Similarly, in sea slugs of the order Sacoglossa, each individual has a penis armed with a stylet. Matings’ are typically reciprocal with slugs circling around each other. Once the sperm is injected it is transported internally where it will be stored in a special sperm storage structure and used to fertilize the recipient’s eggs.

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Figure 2: The sea slug Alderia modesta is hermaphroditic. Each individual has a single penis located on the right side of its body, just behind its head (Image credit: Krug 2007; Angeloni 2003)

Barnacles have a fascinating life-history which involves them remaining fixed to a single spot that they chose as larvae. They mate with other barnacles by extending their long penises (longest in the world relative to body size!) to the opening of another barnacle where they deposit sperm. Thus, the limitations to successful reproduction are on a spatial basis…they can’t mate with another barnacle if that barnacle is out of reach of their penis.

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Figure 3: Barnacles extend their long penises to fertilize each other

In short, many different animal species are simultaneous hermaphrodites, with a few notable exceptions. There are no mammal or bird species that are hermaphroditic, and the only vertebrate examples that we have of hermaphroditism are found in fish, and even here are only present in two species.

The majority of flowering plants make both types of gametes and are either simultaneously hermaphroditic (the same flower makes both seeds and pollen) or are monecious (different flowers on the same plant make seeds and pollen).

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Figure 4: Simple schematic showing three plant sexual systems (Image credit)

For our discussion this week, we read a paper by Eric Charnov, “Simultaneous hermaphroditism and sexual selection,” that was published in 1979.

In this paper, Charnov describes several conditions that would favor the evolution of simultaneous hermaphroditism, resulting in an evolutionarily stable strategy. He notes that a hermaphrodite must ‘pay the cost’ of both sexes, in that a hermaphrodite must make both male and female reproductive structures, including copulatory structures, when present, and gonads. Thus, the resources for reproduction must be split according to whether they contribute to male or female function. In order for hermaphroditism to be favored over separate sexes, the female function of a hermaphrodite must perform half as well (or better) than an individual that is only female. Likewise, the male function must be half as good in a hermaphrodite as it is in a male-only individual. This results in hermaphrodites being equally fit when you combine their male and female functions compared to their separate sex counterparts.

From these relationships, Charnov models the conditions under which we might expect simultaneous hermaphroditism to persist and be favored over separate sexes. A major consideration of this model is that there must be a balance between female and male reproductive functions in order for a hermaphrodite to be as fit as separate sexes. This is shown in Figure 5 below, where for various male fitness values and male resource amounts, we see when hermaphroditism will be favored and when it will not.

During our discussion, Jay Rosenheim suggested thinking of which animals would be best described by the different curves of Figure 5. I’ve added these animals to the figure to illustrate what we came up with. Note the m-value on the graph represents the male gain curve where the specific values are arbitrary, but chosen to show the behavior of the model under different scenarios. For example, a hermaphrodite on the curve with an m value of 1 (which indicates that for every increase in resource there is an increase in male fitness) we imagine sponges or other broadcast spawning animal or a wind dispersed plant. Conversely we imagine a hermaphrodite with an m value of 0.1 (where we get the most bang for our buck with the initial amount of resources, and even with more resources there is little increase in fitness) fits well for a barnacle. As described above, barnacles are sessile animals that copulate with other barnacles that are within the reach of their penis, thus male reproductive success is limited by barnacle density and the addition of more resources to male reproduction doesn’t increase the barnacle’s fitness.  Conversely, the elephant seal provides an interesting example of an animal that increases its fitness only after inputting massive amounts of resources into male reproduction (an m value of 3 on the figure below). Most male elephant seals will never father any young, and those that do must devote the majority of their time to defending their harems and fending off challengers. For elephant seals, hermaphroditism would be a huge disadvantage, with each male having very little remaining resources to devote to egg production or parental care.

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Figure 5: Modified figure from Charnov 1979. Where the y-axis (a) is male fitness, and the x-axis (r) is the input to resources to the male function

Charnov set up several scenarios that describe why hermaphroditism might evolve. The next paper we read gives us a case study of how hermaphroditism might evolve.

Earlier this year, Ola Svensson and colleagues published a paper on a single fish that resulted from a set of experiments they were performing to understand sex determination. When they hybridized two species of fish, most of their offspring resembled either one of the parental species, all except for this one individual, who surprisingly, was hermaphroditic, and even more surprisingly, was self-fertile. In order to self-fertilize, that is, produce offspring using your own eggs and sperm, you must be hermaphroditic. However, not all simultaneous hermaphrodites can self. In fact, many cannot, or show tragic consequences to the health of their offspring when they do. These consequences were seen in this individual fish. This fish was kept in isolation with no prospective mates available, and yet, had a lot of babies. However, about half of this fishes babies died before they reached sexual maturity, as we might expect given the consequences of inbreeding.

All of the observations for this paper took place in the laboratory, and so the question remains whether hybridization that results in a hermaphroditic self-compatible individual could a) occur in nature, and b) would be stable enough to give rise to a new species. Specifically, for question b, could this individual produce enough viable offspring who would then go on to reproduce in a way that gets past the early consequences of inbreeding? The answers to these questions are uncertain….both species of fish (the parental species) do occur in the same place at the same time, so they may be able to hybridize in nature. However, the answer to whether this hybridization could result in a new hermaphroditic species is more difficult to answer with any degree of confidence. Potential hurdles to successful speciation might be due to an inability of the new species to thrive in the parent species environment, maybe they are more susceptible to predation, or less able to tolerate environmental fluctuations. Or there could be genetic incompatibilities between the two parental species that rear their head in the hybrid. However, even given these potential limitations, we shouldn’t disregard the potential for these ‘hopeful monsters’ to arise and be successful, however rare it may be.

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Figure 6: The hermaphroditic and self-fertile hybrid fish (Image credit: Svensson et al. 2016)

-Serena

References

Charnov 1979. Simultaneous hermaphroditism and sexual selection. Proc. Natl. Acad. Sci. 76: 2480-2484. PDF

Krug 2007. Poecilogony and larval ecology in the gastropod genus Alderia. Amer. Malac. Bull. 23: 99-111. PDF

Angelino 2003. Sexual selection in a simultaneous hermaphrodite with hypodermic insemination: body size, allocation to sexual roles and paternity. Animal Behavior. 66: 417–426. PDF

Svensson O., A. Smith, J Garcia_Alonso, and C. van Oosterhout 2016. Hybridization generates a hopeful monster: a hermaphroditic selfing cichlid. Proceedings of the Royal Society B. PDF

 

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