Time for a change: patterns of sex expression, health and mortality in a sex-changing tree

Abstract

Background and Aims The 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. Methods Patterns 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. Results In 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. Conclusions This 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.

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

“…Correlative and experimental studies support the findings that females in striped maple are in poorer overall health (Blake‐Mahmud and Struwe, ) and that severe damage can cue female sex expression. Our study shows that Acer pensylvanicum is a novel and excellent model species for investigations into long‐lived woody plants with ESD.…”

“…These manipulations were (1) crown pruning in May 2015, (2) full defoliation in July 2015, (3) hydraulic restriction through phloem removal in March 2016 and August 2016, and (4) partial defoliation in August 2016. We monitored manipulated and control trees in the flowering seasons of 2015, 2016, and 2017 for sex expression, flowering, and mortality (using methods described by Blake‐Mahmud and Struwe, ).…”

“…Experimental work has indicated that flower sex may be determined within 3 weeks of flowering (Blake‐Mahmud and Struwe, ). Males outnumber females by more that three to one (Hibbs and Fischer, ), possibly as a consequence of high female mortality (Blake‐Mahmud and Struwe, ). Previous studies have shown that in striped maple, deteriorating health correlates with increased female sex expression in individuals (Blake‐Mahmud and Struwe, ) and that branch excision from male trees leads to female‐flowering branches (Blake‐Mahmud and Struwe, ).…”

“…Previous studies have shown that in striped maple, deteriorating health correlates with increased female sex expression in individuals (Blake‐Mahmud and Struwe, ) and that branch excision from male trees leads to female‐flowering branches (Blake‐Mahmud and Struwe, ). The influence of size on sex expression is minimal (Blake‐Mahmud and Struwe, ). However, there are no published causative links between physical trauma and sex expression at the individual level in striped maple or in other Acer species.…”

Death, sex, and sugars: variations in nonstructural carbohydrate concentrations in a sexually plastic tree

“…Recent research has shown that sex expression correlates with overall health. Trees in worse condition (that is, are missing more branches, show more symptoms of infection, or have larger areas of crown dieback) have a higher probability of being female than of being male (Blake‐Mahmud and Struwe, ) Little support has been found for the size‐advantage hypothesis in this species, with both large and small trees expressing the female sex (Hibbs and Fischer, ; Blake‐Mahmud and Struwe, ). The lack of a positive correlation between size and femaleness raises the question of how sex is determined in this species and whether a different metric might better reflect the availability of resources for seed and fruit provisioning.…”