Interview with the author: Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite

Morphological evidence has long supported that simultaneous hermaphrodites invest more into the male sexual function at larger group sizes. In their recent work, Steven Ramm and colleagues use transcriptomic data link this morphological response to gene expression. Learn more about their study below, and in the full paper.

Ramm SA, Lengerer B, Arbore R, et al. Sex allocation plasticity on a transcriptome scale: Socially sensitive gene expression in a simultaneous hermaphrodite. Mol Ecol. 2019;28:2321–2341. https://doi.org/10.1111/ mec.15077

Sex allocation plasticity in Macrostomum lignano from a morphological perspective. The investment into testes (Te, blue) and ovaries (Ov, orange) can be readily quantified in these transparent flatworms (as illustrated in the inset) and used to derive a proxy for sex allocation (as testis area/[testis area + ovary area]). We confirmed that sex allocation varies significantly with the group size treatment (see main text for details). This represents a by now well‐established phenotypically plastic response that we here investigate further from a transcriptional landscape perspective 

What led to your interest in this topic / what was the motivation for this study? 
We’ve long since known about the ability of many simultaneous hermaphrodites to adjust their sex allocation at a morphological level, fine tuning their investment into their male and female sex functions according to cues in their social environment so as to maximise their total fitness returns. More specifically, at larger group sizes, individuals have to compete more to gain fertilisations and it therefore pays to shift investment from their female to their male sex function. The exciting prospect with this study was to be able to link this morphological response to the underlying plasticity in gene expression in organs such as the testis and ovary.

What difficulties did you run into along the way? 
One difficulty in switching from a morphological to a transcriptomic level of analysis was simply the sheer amount of data that we generated. We were measuring gene expression in tens of thousands of transcripts and found thousands of differentially expressed candidates that differed in expression according to the social environment, making it initially difficult to decide how best to focus our follow-up studies of the transcriptomic data.

What is the biggest or most surprising finding from this study? 
For me, one of the biggest surprises was that such a large proportion of the M. lignano genome is differentially regulated in its expression according to the social environment. There are different ways we measured that, but at least 10% of the transcriptome showed evidence for variable expression depending on something as simple as the number of other flatworms they regularly encountered. That’s of course both a blessing and a curse, since we’ve still got a big task ahead figuring out the functional roles of all those genes, and in particular the key gene expression changes within the subset of differentially expressed transcripts that really drive the plasticity.

Moving forward, what are the next steps for this research? 
One thing we’ve already been following up on in some detail is that alongside many transcripts which we expected to be plastically expressed in the testis and ovary (since these are the key organs for sex allocation), we found an additional large class of genes that were also highly plastic in their expression and are predominately or exclusively expressed in the tail of the flatworms. We’ve now found that many of these are expressed in the prostate gland cells responsible for seminal fluid production, another key component of male allocation, opening up the possibility of studying their functional and adaptive significance for sperm competition and sexual conflict.  

What would your message be for students about to start their first research projects in this topic? 
Be realistic about what that project can achieve. The ability to measure gene expression on a transcriptome scale has been a huge boon for the field, and opens up many exciting possibilities. But because we can now measure everything at once, there’s always a risk of drowning in data. If, for example, we would now follow up on all the plastically expressed genes we found in our study, that could easily fill several PhD projects. Clear questions and good experimental design become even more important as technology advances, not less.

What have you learned about science over the course of this project? 
The importance of collaboration. I’ve benefited from working with a great team of people spread across four different countries, which allowed us to combine several different techniques (morphological assays, RNA-Seq, in situ hybridisation, RNAi) in a single study. 

Describe the significance of this research for the general scientific community in one sentence.
Our project has begun to show how the dynamic allocation of resources to producing either sperm or eggs in hermaphroditic organisms occurs at the underlying level of the genes responsible for spermatogenesis and oogenesis, respectively. 

Describe the significance of this research for your scientific community in one sentence.
I hope our research can move sex allocation research forward on a couple of fronts: primarily, it offers a first – though still far from complete – glimpse into the mechanisms of phenotypic plasticity in simultaneous hermaphrodites; and second, it provides the starting point for deciphering the functions of a vast swathe of genes now implicated as being of adaptive significance for either the male or female sex function.

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