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When the going gets tough, the tough turn female: injury and sex expression in a sex-changing tree.

ABSTRACT: PREMISE:Plant sex is usually fixed, but in rare cases, sex expression is flexible and may be influenced by environmental factors. Theory links female sex expression to better health, but manipulative work involving the experimental change of health via injury is limited, particularly in sexually plastic species. A better understanding of mechanisms influencing shifts in sex is essential to our understanding of life history theory regarding trade-offs in sex allocation and differential mortality. METHODS:We investigated the relationship between physiological stress and sex expression in sexually plastic striped maple trees (Acer pensylvanicum) by inflicting damage of various intensities (crown pruning, defoliation, and hydraulic restriction). We then monitored the sex expression of injured and control individuals for 2 years to assess the extent to which injury may cue changes in sex expression. RESULTS:We found that severe damage such as full defoliation or severe pruning increased odds of changing sex to female and decreased odds of changing to male. In fact, no pruned male trees flowered male 2 years later, while all males in the control group flowered partially or fully male. After full defoliation, trees had 4.5 times higher odds of flowering female. Not all injury is equal; less-severe physical trauma did not affect the frequency of sex change to femaleness. CONCLUSIONS:This work demonstrates that physical trauma in striped maple appears to exhibit a threshold effect in which only the most stressful of physiological cues instigate changes in sex expression, a phenomenon previously unknown, and that damage stress is strongly correlated with switching to femaleness. These findings have implications for population sex ratios and sustainability within an increasing stressful climate regime.

SUBMITTER: Blake-Mahmud J

PROVIDER: S-EPMC7155049 | biostudies-literature | 2020 Feb

REPOSITORIES: biostudies-literature

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When the going gets tough, the tough turn female: injury and sex expression in a sex-changing tree.

Blake-Mahmud Jennifer J Struwe Lena L

American journal of botany 20200221 2

<h4>Premise</h4>Plant sex is usually fixed, but in rare cases, sex expression is flexible and may be influenced by environmental factors. Theory links female sex expression to better health, but manipulative work involving the experimental change of health via injury is limited, particularly in sexually plastic species. A better understanding of mechanisms influencing shifts in sex is essential to our understanding of life history theory regarding trade-offs in sex allocation and differential mo ...[more]

PMID: 32086802

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Project description:Background and aimsThe ability of individuals to change sex during their lifetime is known as environmental sex determination (ESD). This represents a unique life history trait, allowing plants to allocate resources differentially to male and female functions across lifetimes, potentially maximizing fitness in response to changing environmental or internal cues. In this study, Acer pensylvanicum, a species with an unconfirmed sex determination system, was investigated to see what patterns in sex expression existed across multiple years, if there were sex-based differences in growth and mortality, and whether this species conformed to theoretical predictions that females are larger and in better condition.MethodsPatterns of sex expression were documented over 4 years in a phenotypically subdioecious A. pensylvanicum population located in New Jersey, USA, and data on size, mortality, health and growth were collected. A machine-learning algorithm known as a boosted classification tree was used to develop a model to predict the sex of a tree based on its condition, size and previous sex.ResultsIn this study, 54 % of the trees switched sex expression during a 4-year period, with 26 % of those trees switching sex at least twice. Consistently monoecious trees could change relative sex expression by as much as 95 %. Both size and condition were influential in predicting sex, with condition exerting three times more relative influence than size on expressed sex. Contrary to theoretical predictions, the model showed that full female sex expression did not increase with size. Healthy trees were more likely to be male; predicted female sex expression increased with deteriorating health. Growth rate negatively correlated with multiple years of female sex expression. Populations maintained similar male-skewed sex ratios across years and locations and may result from differential mortality: 75 % of dead trees flowered female immediately before death.ConclusionsThis study shows conclusively that A. pensylvanicum exhibits ESD and that femaleness correlates with decreased health, in contrast to prevailing theory. The mortality findings advance our understanding of puzzling non-equilibrium sex ratios and life history trade-offs resulting from male and female sex expression.

Project description:BackgroundTeleost fishes exhibit remarkably diverse and plastic sexual developmental patterns. One of the most astonishing is the rapid socially controlled female-to-male (protogynous) sex change observed in bluehead wrasses (Thalassoma bifasciatum). Such functional sex change is widespread in marine fishes, including species of commercial importance, yet its underlying molecular basis remains poorly explored.MethodsRNA sequencing was performed to characterize the transcriptomic profiles and identify genes exhibiting sex-biased expression in the brain (forebrain and midbrain) and gonads of bluehead wrasses. Functional annotation and enrichment analysis were carried out for the sex-biased genes in the gonad to detect global differences in gene products and genetic pathways between males and females.ResultsHere we report the first transcriptomic analysis for a protogynous fish. Expression comparison between males and females reveals a large set of genes with sex-biased expression in the gonad, but relatively few such sex-biased genes in the brain. Functional annotation and enrichment analysis suggested that ovaries are mainly enriched for metabolic processes and testes for signal transduction, particularly receptors of neurotransmitters and steroid hormones. When compared to other species, many genes previously implicated in male sex determination and differentiation pathways showed conservation in their gonadal expression patterns in bluehead wrasses. However, some critical female-pathway genes (e.g., rspo1 and wnt4b) exhibited unanticipated expression patterns. In the brain, gene expression patterns suggest that local neurosteroid production and signaling likely contribute to the sex differences observed.ConclusionsExpression patterns of key sex-related genes suggest that sex-changing fish predominantly use an evolutionarily conserved genetic toolkit, but that subtle variability in the standard sex-determination regulatory network likely contributes to sexual plasticity in these fish. This study not only provides the first molecular data on a system ideally suited to explore the molecular basis of sexual plasticity and tissue re-engineering, but also sheds some light on the evolution of diverse sex determination and differentiation systems.

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When the going gets tough, the tough turn female: injury and sex expression in a sex-changing tree.

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When the going gets tough, the tough turn female: injury and sex expression in a sex-changing tree.

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