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To band or not to band: what drives the expression of fashion accessories in female pipefish?

“Tale as old as time.
Female chooses male.
Male is large in size.
Male has weaponry.
Unsurprisingly!

Male’s ornamentation.
Male’s behavior.
Female makes the eggs.
Takes care of the young.
Male and female roles.”1
But not all the time!

1Adapted from Disney’s “Beauty and the Beast” written by Howard Ashman
© Dr. Emily Rose

As the female is usually in charge of some degree of parental care, she gets to be picky with whom she mates. Males are often elaborately decorated, especially during mating season. However, in some species, females can be under stronger sexual selection. In these cases, the female is the one putting on a show for the male and it is the male that then takes care of the offspring.

It is intriguing that closely related species do not consistently have sex-role reversal. Some have males expressing genes responsible for the sexual dimorphism (often regulated by hormones, such as androgens and estrogens), while in other species, it’s the females. As males and females share most of their genome, differential gene expression is often controlled by other factors, such as the aforementioned hormone levels. If androgen leads to male ornamentation, estrogen is likely the driving factor for female ornamentation or mating behavior.

One way to explore the mechanisms that drive differences in males and females in sex-role reversed species is to look at genes that are responsible for sexual dimorphism. If these differences are driven by estrogen, estrogen response elements (EREs; these unlock the expression of genes), are expected to be in higher abundance in the vicinity of genes involved in sex-specific morphological characteristics and behavior. Males would of course have the same EREs. In fact, they would start showing the same features expressed in females if they were exposed to estrogen.

© Nicole Tosto

Anderson et al. (2020) used the Gulf pipefish to investigate the drivers of certain sexual dimorphism characteristics. Gulf pipefish females display transverse iridescent bands on the sides of their body and have deeply keeled abdomens.

The authors used transcriptomic analyses of skin and muscle tissues, accompanied by an annotated genome. In order to identify important genes, some male pipefish were exposed to estrogen, other males were not, and tissue samples from females not exposed to additional estrogen were analyzed for their up-regulated genes.

Overall, they found that 28 genes in skin and muscle tissue differed in their expression between estrogen exposed and non-exposed males. They also consistently found an enrichment of the EREs near these genes in males, estrogen-exposed males, and females.

The group was able to identify potential functions of a variety of genes responsible for iridophore formation, coloration, and banding patterns, as well as for the arrangement and distribution of cells in the extracellular matrix. The function of those genes in the Gulf pipefish were inferred from studies on other organisms, often fish. Therefore, their function so far can only be hypothesized – a great starting point to an array of new studies. A few genes were up-regulated in the estrogen-exposed males, but not in females. These genes were mostly associated with muscular and structural functions and as females already exhibit a deeply keeled abdomen, it is hypothesized that only estrogen males would be expressing those genes in response to estrogen.

Another interesting up-regulated gene in the females as well as estrogen-exposed males is associated with supporting prolonged anaerobic respiration. Females in species like the Gulf pipefish exert more energy for courtship behavior. The same up-regulated gene has also previously been shown to be involved in the formation of tissue for the storage of fat and therefore energy reserves likely needed for courtship and the production of eggs. The authors hypothesize that this may be the case here as well. In other species, where males court and have ornaments, estrogen has the opposite effect on a lot of the above-mentioned genes.

This study supports that certain features differentiating males from females, like ornamental accessories, are not pre-determined during early developmental stages when the body plan of the organism develops in response to which sex chromosomes it has. In this particular case, if males are exposed to estrogen, the cells in their body react by expressing genes that over time morphs the male into a female-like appearance. There clearly is a lot more to sexual dimorphism accessories than meets the eye!

Reference

Anderson AP, Flanagan SP, Rose E, Jones AG. 2020. The estrogen-responsive transcriptome of female secondary sexual traits in the Gulf pipefish. Journal of Heredity 111: 294-306.

 

Sabrina Heiser (@SabrinaHeiser) has written blog posts in Dr. Stacy Krueger-Hadfield’s Conservation Genetics and Science Communication courses at the University of Alabama at Birmingham. She is pursuing a PhD in Dr. Chuck Amsler’s lab. She is passionate about science communication, and, therefore, takes any opportunity she can to advance her skills. Her current research focuses on the evolutionary processes generating and maintaining diversity in a red macroalga in Antarctica. You can read more about the research she has been involved in on UAB in Antarctica or get a glimpse of what else she is up to on her website.

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