Sexual dimorphism and pattern of resource allocation under variable abiotic factors

1 Introduction

Dioecy is one of the most fascinating sexual systems among plants, offering vast scope for research pertaining to reproductive biology, genetics, physiology, and related fields (Barrett, 2010). Dioecy is widely distributed across angiosperm clades and in approximately 6% of the flowering plants (Renner, 2014). Studies have variously highlighted ecological-evolutionary factors such as resource allocation strategies, habitat, and wind-pollination are key to understand the evolution and maintenance of dioecy (Renner, 2014; Mangla et al., 2020; Pannell and Jordan, 2022). To maximize reproductive output, dioecious plants often display bias between the paternal versus maternal functions for available resources, which plays a vital role in the evolution of dioecy. The biased partitioning of resources results in differences in morphological, physiological, and life-history traits between sexes, which thereby exhibit sexual dimorphism (Geber et al., 1999; Obeso, 2002). In the later stages of evolution, sexual dimorphism becomes essential for the maintenance of dioecy (Geber et al., 1999; Barrett and Hough, 2013). In the literature, terms “secondary sexual dimorphism” and “secondary sex characteristics” have been occasionally used to describe these differences between sexes. These terms distinguish the vegetative features, life-history traits, and so forth of male and female plants from floral organ differences (stamens vs. pistil—primary sex characteristics) (Geber et al., 1999; Barrett and Hough, 2013). However, studies also present sexual dimorphism among dioecious taxa in their vegetative, reproductive, and eco-physiological traits, together with use of the term “sex-specific characteristics” rather than “secondary sexual dimorphism” (Geber et al., 1999; Ashman, 2005; Dudley, 2006; Hesse and Pannell, 2011; Barrett and Hough, 2013; Juvany and Munne-Bosch, 2015; Retuerto et al., 2018; Liu et al., 2021).

Sexual dimorphism is not merely an intrinsic balance of available resources to a species and between sexes; rather, it reflects the interplay of abiotic factors such as light, wind, and water with them (Godoy et al., 2011; Juvany and Munne-Bosch, 2015; Tonnabel et al., 2014; Liu et al., 2021), which also balances the directionality of evolution (Barrett and Hough, 2013; Tsuji and Fukami, 2020). A recent meta-analysis has demonstrated that drought significantly increases root mass but decreases stem, leaf, and reproductive mass (flowers, fruit, and seed mass). The roots of herbaceous plants are more sensitive to drought than those of woody plants, with the latter showing a sharp reduction in reproductive allocation (Eziz et al., 2017). Such adaptations shape sex-specific physiological strategies, resource allocation, and reproductive success; for instance, females exhibit higher root mass in Mercurialis annua than males (Hesse and Pannell, 2011). Male and female plants often differ in photosynthetic efficiency, stress tolerance, and growth patterns, depending on light intensity, quality, and water availability (Geber et al., 1999; Rakocevic et al., 2023, 2025). These factors modulate the life history traits of dioecious taxa and thus direct vegetative allocation, reproductive efforts, and reproductive output (Obeso, 2002; Dudley, 2006).

In dioecious taxa, both sexes exhibit adaptive plasticity in resource allocation (i.e., differential plasticity hypothesis; Obeso, 2002; Delph and Bell, 2008), enabling the survival and modulation of reproductive strategies under abiotic stress conditions (Dudley, 2006; Retuerto et al., 2018). Owing to plasticity in resource allocation, males and females may respond differently to environmental heterogeneity (Nicotra et al., 2010). As a general trend among dioecious taxa, vegetative and reproductive resource requirements differ between sexes. Males tend to invest more in their vegetative growth and have a larger clone size than females. Moreover, males invest heavily in flower and pollen production, whereas females produce fewer flowers and allocate more resources to seed and fruit production. This resource allocation strategy exhibits a differential vegetative and reproductive allocation of resources in males to maximize reproductive efforts through the effective dispersal of pollen. In contrast, female reproductive efforts maximize seed set by ensuring mate availability and siring success (Geber et al., 1999; Obeso, 2002; Hesse and Pannell, 2011; Barrett and Hough, 2013). As females require greater allocation for reproduction than males, this may suggest that females exhibit low biomass assimilation and growth (e.g., M. annua—Sánchez Vilas and Pannell, 2011, Bürli et al., 2022; Jhajhariya et al., 2024). However, studies in Salix planifolia and other Salix species reported similar growth rates in both male and females (Turcotte and Houle, 2001; Sakai et al., 2006). Nonetheless, the vegetative and reproductive phase may be differentially impacted by the same environmental factor, even amongst the same sex (Delph and Bell, 2008; Sánchez Vilas and Pannell, 2011; Tonnabel et al., 2017; Teitel et al., 2016; Retuerto et al., 2018).

The key life-history traits associated with dioecy include clonality, sex-ratio, and the spatial segregation of sexes (Renner and Ricklefs, 1995; Vallejo-Marín et al., 2010; Mangla et al., 2020). These are also strongly influenced by abiotic and biotic factors (e.g., competition, herbivory) (Juvany and Munne-Bosch, 2015; Liu et al., 2021) and are intrinsically connected with the extent of sexual dimorphism (Geber et al., 1999; Barrett and Hoguh, 2013; Mangla et al., 2020). In relation to resource allocation and ecological context, niche divergence/specialization, sex-ratio, the spatial segregation of sexes, and physiological specialization have been investigated as ecological correlates of sexual dimorphism (Dudley, 2006). For example, temperature acts as a limiting factor for sexual reproduction and may promote clonal propagation in dioecious species, thus altering sex-ratios. An example is elevated temperature increases males in herbaceous Valeriana edulis (Petry et al., 2016) and females in woody Populus cathayana (Chen et al., 2021). It is noteworthy that the effects are species-specific. Another example is water availability; generally, female plants prefer mesic, nutrient-rich sites whereas males are often present in xeric sites with limited resources. This kind of strategy exhibits the spatial segregation of sexes and may imply niche divergence or specialization. However, this generalization has been tested, and studies have shown deviation at least once, considering the sex-ratio of natural populations and inter- and intra-sex competition within natural populations (Dudley, 2006; Galfrascoli and Calvino, 2020).

The environmental drivers of dioecy enhance the extent of sexual dimorphism. Nonetheless, generalizations are not always valid, as the plasticity exhibited by plants/sexes is species-specific (Obeso, 2002; Dudley, 2006; Tonnabel et al., 2017). Moreover, this plasticity is widely expected to pose evolutionary consequences (Geber et al., 1999). A comprehensive review of sexual dimorphism in relation to abiotic factors would bring recent advanced evidences together to make generalizations (if any) and highlight variations of such responses across species. In addition, the differential abilities of sexes to utilize light and respond to stress can shape niche and community dynamics. Thus, these understandings may help shape conservation strategies and agroforestry restoration. This review outlines the impact of abiotic factors in relation to sexual dimorphism and sex-specific strategies for the effective utilization of available resources.

2 Abiotic factors: consequences on dioecy and sexual dimorphism

2.1 Drought/water conditions

Drought is one of the chief stressors of land plants. In the scenario of climate change, the frequency/severity of drought may be increased (Ferreira et al., 2015; Eziz et al., 2017). The spatial segregation of sexes in relation to water availability is quite apparent in the literature (Figure 1). As the sexes may experience water conditions differently, it is first considered here.

The relationship of the spatial segregation of sexes with water reflects the concept of dimorphic niche (Dudley, 2006) and different resource allocation strategies between sexes (Barrett and Hough, 2013). For example, dwarf willow (Salix arctica) female plants are frequent in mesic, nutrient-rich habitats while males are present in xeric, nutrient-poor sites (Geber et al., 1999). Jhajhariya et al. (2024) observed a similar pattern in Hippophae rhamnoides for water availability related to sex distribution: females preferred mesic sites while males were dominant in xeric sites. Likewise, studies on a Chinese population of H. rhamnoides suggested that at higher altitudes, water stress induces a negative impact on females through poor growth and greater mortality (Li et al., 2004; Li et al., 2007). These two studies on H. rhamnoides suggest dimorphic niche specialization in the species, which will require detailed investigation. Interestingly, the pattern of resource allocation does not change with respect to habitat change within a sex in natural populations (Jhajhariya et al., 2024).

Studies have demonstrated that a dimorphic niche can significantly influence resource allocation and sexual dimorphism. In particular, sex-specific adaptive strategies (for resource allocation and survival) and the spatial segregation of sexes can be observed in relation to water. First, a well studied example is Salix glauca, where the spatial segregation of sexes was observed with relation to habitat variation or mesic versus xeric sites (Dudley, 2006). Both sexes exhibited reduced growth rates in xeric sites compared to mesic sites. However, female growth rates at xeric sites were significantly lower than for males. These results suggest that female growth and resource allocation depends on water availability. It is likely that limited water availability diminishes nutrient uptake and photosynthetic ability, especially in females. Hence, females exhibit a trade-off for vegetative growth over reproduction. A second strategy observed was that, despite having greater reproductive cost, females produced more leaves before fruit maturation to meet the mandatory carbon requirement to support fruit development and survival for the next season (e.g., in Hebe subalpina; Delph, 1990). Another strategy where, in an attempt to maximize reproduction, females exhibit trade-off for example in Pistacia lentiscus, where resource allocation for reproduction is achieved by conserving vegetative allocation (Correia and Diaz Barradas, 2000). In this species, both fruit formation and leaf development occur during summer in a water-limited environment. Females, however, retain older leaves and also reduce the production of new leaves compared to males; this appears to be a strategy of trade-off and may be to avoid stress.

At inter- and intra-population levels, sex ratios are greatly influenced by water content/availability. For an instance, under drought conditions, higher growth rate and clonality in female Acer negundo leads to female-biased sex ratios, attributed to greater root development that can access ground water and provide a buffering ability to withstand water scarcity more than males (Dawson and Ehleringer, 1993). A similar recent study found that A. barbinerve male vegetative growth was significantly impacted by environmental stress (especially water), while females maintained relative stability and growth (Liao et al., 2025). In contrast, female Populus cathayana are more sensitive to drought than males (Chen et al., 2021), and a higher male bias sex-ratio has been found at higher altitudes and was correlated with water availability (e.g., in A. negundo, Hesperochloa kingii, and Distichlis spicata) (Field et al., 2013a, Field et al., 2013b). Even in aquatic environments, water depth affects clonal reproduction and sex ratio (e.g., in Vallisneria sp.) in conjunction with light availability (Li et al., 2019; Zhou et al., 2019).

It can be inferred from the above-cited studies that niche specialization/sex-specific strategies ensure and maximize reproductive output. The consequence of water stress/drought may be differential for male and female plants. The prevalent examples indicate that males are more severely affected than females under water stress as they already prefer or are specialized to grow in xeric sites. Moreover, drought/water stress may affect dioecious taxa at different levels (individual level, population level).

2.2 Light

The growth form (vertical vs. horizontal growth) and habitat of a plant (land vs. aquatic) may exhibit a variable pattern of light capture and responses. As the tallest plants may remove/capture a large proportion of the light resource, light thus provokes a peculiar asymmetrical competition in plants (tall vs. short). That competition leads to plastic responses in light scarcity, a response known as “shade-avoidance”, which is overcome by an increase in plant height through internode elongation and reduced branching (Schmitt and Wulff, 1993; Sleeman et al., 2002). Physiologically, this phenomenon occurs due to changes in the light spectrum: as daylight passes through vegetation, the R–FR ratio lowers due to absorption of red by photosynthetic pigments. From a resource allocation viewpoint, the vertical growth of plants is achieved by higher resource allocation, while there is a trade-off with reduced reproduction and total biomass. In the context of dioecious plants, Tonnabel et al. (2017) found for the annual herbaceous Mercurialis annua that at higher density, the mean length of the plant and its first branch, plant diameter, and biomass were lower both in males and females. Indeed, higher density (hence, light limitation) reduced the relative reproductive allocation and efforts in females more than in males. This suggests a greater trade-off in females both for vegetative and reproductive allocation at higher densities and light-limiting environments. This may be considered a female sex-specific strategy to maximize current reproductive success in terms of carbon acquisition and seed maturation. Nonetheless, it is highlight that at higher density, typical shade-avoidance responses may not be elicited, but negative effects of light limitation may appear.

Another study, on Hippophae rhamnoides, a species growing in the cold desert of India (Leh-Ladakh region), exhibited sexual dimorphism, with most of its vegetative traits and reproductive traits aligned to support wind pollination (Mangla and Tandon, 2014; Jhajhariya et al., 2024). The species grows as gregarious dense patches due to immense clonal propagation. The extent of sexual dimorphism does not change, even when male and female patches are mixed or discrete. However, both sexes exhibit plasticity to maximize reproductive effort and output by producing less flowers and vegetative growth, while males produce flowers as much as twice the rate of females, attaining a greater height. Because the species grows in open terrain with high light intensity (optimal for the species), no competition for light is observed, and hence no negative outcomes for light limitation are apparent (personal observations) (Jhajhariya et al., 2024).

Under optimal growth and light conditions, sex-specific physiological responses may not appear. However, under stress, sex-specific responses and strategies to overcome it may be apparent between sexes (Retuerto et al., 2018; Trancoso et al., 2025). For an instance, in Pistacia lentiscus (undercanopy small tree-shrub), no difference in photosynthetic activity/capacity is apparent between male and female plants, but under low irradiance, males show higher quantum yield or photosynthetic efficiency and higher carbon assimilation than females (Correia and Diaz Barradas, 2000). Likewise in Amaranthus palmeri, the sexes show no physiological differences (total chlorophyll content) when allowed to grow under ambient white light with low or even medium intensity. However, under high light intensity, female plants possess lower chlorophyll content than males, exhibiting higher and early flowering than males to maximize reproduction (Korres et al., 2017, Korres et al., 2023). Such results suggest that males are relatively more tolerant to light stress than females. On the other hand, in the context of biomass and nutrient assimilation among males and females, such as in dioecious perennial herb Rubus chamaemorus, N and P content were higher in aboveground biomass of both the sexes under open habitat conditions compared to individuals growing in the shade (Ågren, 1988). This suggests that R. chamaemorus exhibits similar sex-specific strategies to resource allocation under variable light conditions.

Recent studies have indicated the differential impact of light stress (photoinhibition, photooxidation, etc.) upon the life-history stages of each sex, such as in the dwarf palm Chamaerops humilis, which grows in Mediterranean-type ecosystems, and experience warm-dry summers and wet-mild winters (Morales et al., 2016). Females exhibit lower water content in leaves and higher photoinhibition than males only during warm-dry summers. The mature plants of both sexes comprise more carotenoid content than juvenile plants and other stress combating molecules. This suggests that only females are affected by high light conditions but supports the reproductive phase by lowering leaf-water content. In contrast, the leaves of female Ilex paraguariensis show a higher photosynthetic rate than males, which is expressed during vegetative stages before flowering and fruit ripening (Rakocevic et al., 2011). Nevertheless, at experimental monoculture (high light, such as open canopy) and agroforestry (low light conditions, such as understory forest) conditions, lower sensitivity of females to extreme light conditions than males was found, owing to higher Chl b index and lower Chl a/b ratio (Rakocevic et al., 2025). Even in A. palmeri, the Chl a/b ratio is lower at higher light intensity in females than males (Korres et al., 2023), suggesting a shade-adapting trait of the species.

Available recent studies on aquatic macrophytes provide a chance to compare the response of dioecious land plants with dioecious aquatic plants. For instance, in the aquatic macrophyte Vallisneria spinulosa in shallow (high light) and deep (low light) water, females exhibit a proportional decline in allocation to reproduction. However, male allocation for reproduction was similar at all depths. In comparison to males, females invested a higher proportion of resources to sexual reproduction at all water depths investigated. This suggests that females exhibit greater plasticity for biomass allocation and reproduction attributed to light (Li et al., 2019). An another study found that V. natans females display more phenotypic plasticity than males with respect to light conditions and water depth in terms of leaf length, vegetative biomass, and reproductive allocation. All the measured vegetative (leaf size, total biomass, etc.) and reproductive traits exhibited sexual dimorphism, and the degree was higher in females than males for all traits. With changes in water depth, the leaf size, total biomass, and the biomass of reproductive organs shows significant variation in females compared to males. For example, at higher depths and low light conditions, females decrease their leaf length, spathe number, and flowering ramet (Zhou et al., 2019). In both species of Vallisneria, the sexes exhibit equal investment in clonal propagation via tubers/stolon at all water depths, but the trade-off for sexual reproduction was evident only in females (Li et al., 2019; Zhou et al., 2019). Such observations reiterate that, as in land plants, females exhibit more plasticity to ensure reproduction, even in aquatic environment.

Intriguingly (and in contrast to land dioecious plant), the rate of photosynthesis increased in Vallisneria males and females with increasing water depths and hence low light conditions. This suggests that in shallow water, high light intensity potentially causes light inhibition, and at 1.3 m deep, available light is not limited for photosynthesis. Here, it is important to note that in V. natans, males maximize reproductive effort and efficiency by producing more flowers than females. Females exhibit reduced vegetative and reproductive allocation by reducing leaf size, spathe number, and flowers by maintaining photosynthetic rates at each depth. Hence, resources (e.g., carbon) are reserved and are allocated to seed and fruit production (Zhou et al., 2019). These studies corroborate sex-specific adaptive strategies in aquatic plants, aligning with the theory of differential plasticity as documented in woody and herbaceous dioecious taxa.

Research targeting resource allocation pattern under light conditions indicates that sex-specific physiological responses usually increase/become more pronounced in stressful environment, especially in low light and light-competing environment. These studies make any generalization difficult, as sexes that exhibit different responses for the same factor may be dependent on the life-history stage and a great extent of plasticity in dioecious taxa to ensure reproduction. Here, it may be proposed that as female bear higher reproductive investment, they thus have better resource allocation strategies/adaptations to provide reproductive assurance, even under stress conditions.

2.3 Soil and carbon (C), nitrogen (N), and phosphorous (P) allocation

The differential resource allocation pattern to each sex may also be indicated by nutrient availability in vegetative and reproductive parts. The currencies used for such estimations are C, N, and P. Research indicates that C-based resources are more limiting than N for plants; it is generally accepted that it is the “best” currency to use when assessing resource allocation in limiting environment/habitat (Reekie and Bazzaz, 1987; Hesse and Pannell, 2011). In general, females rely heavily on C, N, and water for fruit/seed production, while males invest more N for pollen production; thus C may be less limiting for male reproduction (Geber et al., 1999; Ishida et al., 2005). For example, in plants such as Siparuna grandiflora (Siparunaceae), a tropical dioecious shrub (Nicotra, 1999), Lithraea molleoides (Anacardiaceae) (Galfrascoli and Calvino, 2020), etc. greater N allocation has been computed for females in flower and fruit production than in males. In the dioecious perennial herb Rubus chamaemorus, female flowers had a lower dry mass and nutrient content than male flowers. However, the N and P content of fruit was many times that of male flowers (Ågren, 1988). Salix glauca females show approximately a four times higher allocation of P than males. However, N allocation budgets did not differ significantly between sexes in species (Dudley, 2006). Female Amaranthus palmeri plants also accumulated higher amounts of minerals N, P, K and Mg in their stems (including inflorescences) than male plants (Korres et al., 2023). These sexual differences in the allocation of C and N and other elements between sexes support the generalization that these all likely contribute to sexual size dimorphism (Sánchez Vilas and Pannell, 2011). Interestingly, higher allocation in females clearly demonstrates the higher cost of reproduction in females and a female-specific strategy to allocate seed filling and fruit formation.

Nevertheless, few studies have investigated nutrient availability in soil and its utilization with respect to resource allocation (both vegetative and reproductive) pattern. Differential resource allocation strategies between sexes may be driven by soil nutrient content and its utilization (Hesse and Pannell, 2011; Jhajhariya et al., 2024). However, studies have indicated that the size disparity between the sexes in terms of biomass is not greatly affected by soil nutrient availability. For example, M. annua males decrease their reproductive allocation, but females do not on nutrient-poor soils. This may be due to selection favoring plasticity in reproductive allocation and/or relative higher allocation towards the roots, which balances nutrient limitation (Geber et al., 1999; Hesse and Pannell, 2011). Soil and the shoots of male and female H. rhamnoides exhibited similar C and N content during the flowering season. The C and N content of the soils of females declined significantly during fruiting season, again indicating a heavy allocation of resources to fruit by females (Jhajhariya et al., 2024).

Factors such as stress and competition may affect resource allocation patterns differentially between the sexes. For example, M. annua females in light limiting environments exhibit a decline in reproductive efforts and hence reduced allocation to reproduction than males; this is attributed to less carbon availability (Tonnabel et al., 2017). In contrast in H. rhamnoides, C and N content in vegetative parts (leaves and shoots) do not vary between the sexes, highlighting the absence of a soil-nutrient-based trade-off among the sexes for vegetative and reproductive functions (Jhajhariya et al., 2024). The study corroborated soil nutrient availability and suggests that the overall decline in total C and N content in soil during fruiting is obvious as the vegetative growth phase, fresh leaf-flush, and fruiting phase are overlapping in the species. Such resource-allocation strategies highlight that the sexes attempt to optimize their respective fitness under given ecological conditions.

2.4 Temperature

Few studies have investigated the effect of elevated temperature (in the context of climate change) on sex-specific strategies and responses among dioecious taxa. Relevant studies have suggested that temperature regimes may influence vegetative (bud break) and reproductive phenology and the physiology of dioecious taxa in a sex-specific and/or species-specific manner. The effects are species-specific and even variable within a genus, as in Populus, a well investigated taxon. In P. tomentosa, females exhibit better adaptation to high temperatures than males (Song et al., 2014). However, P. trichocarpa shows no intersexual differences for changing (increased) temperature. Remarkably, recent experimental manipulations on P. cathayana have indicated that females of the species appear more sensitive to elevated temperature and drought while males are positively affected by elevated carbon dioxide levels (Chen et al., 2021). The limited extent of research restricts drawing any unifying model or generalization in this aspect.

It has been variously suggested that temperature chiefly influences the optimal C balance (via altered carbon cycle, production of secondary metabolites, etc.) and hence, resource allocation patterns (growth, biomass allocation, etc.) among dioecious taxa (Klein et al., 2025; Chen et al., 2021; Zhao et al., 2024). Sex-specific changes in response to climate change may also induce sex-specific mortality, leading to altered/skewed sex-ratios or eco-physiological specialization in one sex or its failure, which could eventually affect the population’s survival by declining reproductive success and fitness of the species (Hultine et al., 2016, 2018). Thus, higher levels of stress may cause female mortality and a male-biased ratio in a population, which may push it toward reproductive failure (Field et al., 2013a; Field et al., 2013b).

The incidence of bioclimatic variables, especially temperature, influencing sexual dimorphism is present in Rumex hastatulus and is found to positively correlated (Puixeu et al., 2019). Populations from sites with higher mean annual temperatures had greater male- and female-biased sexual dimorphism, especially in vegetative traits. A higher investment of resources was found for stems in males than in females (i.e., male dimorphism for plant height). On the other hand, female dimorphism was evident for higher leaf production at maturity, highlighting greater investment by females in leaves under higher temperatures (Puixeu et al., 2019). Warming also results in yielding higher total biomass and nutrient pools, root growth, and enhanced photosynthetic performance in female plants of Morus alba (Wang et al., 2026).

In dioecious plants, the differential extent of clonality between male and female plants leads to deviation from the ideal 1:1 sex-ratios in natural populations (Field et al., 2013a; Field et al., 2013b). Such biased sex ratios profoundly modulate sexual dimorphism and interactions with abiotic (nutrient availability, light, etc.) and biotic (especially competition) factors (Renner and Ricklefs, 1995; Vallejo-Marín et al., 2010; Mangla et al., 2020). Evidence (though limited) indicates that temperature regimes may affect clonality and the extent of sexual reproduction in diclinous taxa. For example, in the clonal tristylous aquatic plant Decodon verticillatus, populations are distributed at the northern and southern range of eastern North America. At northern range species have mostly lost the ability to sexually reproduce, and clonal propagation is widespread to the extent that the whole population is represented by single genotype. However, southern populations exhibit seed set only by sexual reproduction. Glasshouse studies on the species have shown more winter survival of sterile clones than fertile clones from the northern range (Eckert, 2002). This suggests temperature as a limiting factor for sexual reproduction in northern range limits of the species but supports clonal propagation. Clonality in dioecious plants also reflects resource allocation strategies in below-ground structures level such as runners and tubers. It has been observed that high temperatures favor clonal propagation, especially in males, and limit the extent of sexual reproduction under unfavorable conditions. Moreover, clonal offspring are proven to be of better adaptive plasticity than sexual offspring in the hermaphrodite Fragaria vesca (Sammarco et al., 2025). This needs to be tested further in dioecious taxa.

The effect of temperature on the sex ratio of the dioecious plants is indirect. An interesting study on the alpine dioecious herb Valeriana edulis (Caprifoliaceae) investigated the long-term impact of climate change on its sex ratio and the reproductive performance in 31 populations (Petry et al., 2016). Climate warming has affected the sex ratio in the species, and in the last 4 decades female biasness has increased. The reason for this is the shift in the species towards a higher altitudinal gradient due to the availability of moisture (due to snow melt) and suitable temperature regimes. In contrast, the area occupied by the male plants had declined significantly along with their numbers. The skewed sex ratios, absence of males in some populations, and presence of only-male populations (at higher altitudes) have drastically reduced seed-set and reproductive output. Other unisexual taxa may also serve as the key examples in this regard, such as in cucumbers (Cucumis sativus, monoecious), where temperature affects the node position of female flowers and thus the ratio of male to female flowers. High temperatures promote male flower differentiation while low temperatures usually induce female flowers (Luo et al., 2023). Likewise, mangoes (Mangifera indica, andromonoecious) exhibit higher proportions of hermaphrodite flowers at low temperatures, and at high temperatures the sex ratio in inflorescence becomes female biased (Shü, 1999). It could be ascertained here that the sex-specific strategy for water availability (as highlighted the Section 1.1) along with temperature are key drivers in maintaining reproductive assurance and success in a dioecious species.

2.5 Salinity/alkalinity stress

Increasing salinity/alkalinity in soil due to excess flooding, anthropogenic factors, and climate change is emerging as a stressor of plants. Alkalinity breaks the nutrient availability continuum between plant roots and the soil, causing ionic imbalance and hence affecting plants’ vegetative and reproductive fitness (Rao et al., 2023; Liu et al., 2026). Accompanied by other stressors such as drought, the consequences become more complex. In dioecious plants, these consequences may be multifaceted, as each sex may respond differently to this physiological stress, which may lead to the exclusion of one gender from the population, resulting in skewed sex ratios. This stress may also affect the pattern of resource allocation and extent of sexual dimorphism. Available studies on Populus, Salix, and Spinacia oleracea provide valuable insights into understanding the sex-specific strategies to this stress (Melnikova et al., 2017).

In Populus tomentosa, (on stem-cuttings) under the combined effect of salinity and water stress, females suffered a higher reduction in leaves, stems, biomass, and total leaf area than males (Lu et al., 2018). Similarly, in P. deltoides, females exhibited growth inhibition, reduction in root biomass, and damage to roots under salinity stress. Females also exhibited a lower ability of reactive oxygen species (ROS) scavenging than males (Hao et al., 2020). The study exhibited differential trade-offs for growth and functional traits between the sexes, especially in females, as a reduction in the above traits enable males to better survive in limited environments/stress. In contrast, Feng et al. (2020) found in investigating salinity stress in Salix linearistipularis that male and female stem cuttings revealed differential physiological response and its avoidance strategies. Compared to male leaves, female leaves exhibited higher superoxide dismutase and peroxidase activities (ROS scavenging activities), higher photosynthetic capacity, and lower H₂O₂ content. Sodium ion (Na⁺) accumulation was lower in female leaves. These results suggest that female cuttings were more tolerant than males to salinity stress due to higher ROS scavenging and lower leaf Na⁺ accumulation in female leaves and higher root Na⁺ efflux capacity than males.

3 Physiological specialization between sexes and cross-taxa generalization: a dilemma

The extent of physiological specialization between sexes may provide a fundamental strategy to study the ecological and evolutionary maintenance of dioecy. It is hypothesized that weak sexual dimorphism reflects early evolutionary stages of dioecy (Cossard et al., 2018; Perez-Llorca et al., 2024). However, this needs further testing. Existing studies on sex-specific strategies and responses to diverse abiotic factors have examined variation in growth and nutrient allocation along with intrinsic physiological parameters across different ecosystems (terrestrial and aquatic) and patterns of competition (inter and intra sex) for resources (Nicotra, 1999; Eppley, 2001; 2006; Barrett and Hough, 2013). Though competition is a biotic factor, it is an integral part of abiotic factors interactions. This aspect is dealt briefly in a separate section. The physiological parameters used to understand physiological specialization in dioecious taxa include water use efficiency, photosynthetic efficiency/rate, photosynthetic N-use efficiency, stomatal conductance, chlorophyll a and b content, the chlorophyll a/b ratio, specific leaf area, and root development/mass (Chen et al., 2021; Korres et al., 2023; Trancoso et al., 2025) (Figure 1). These parameters exhibit plasticity and assume to play key roles in adaptations in a sex-specific manner (e.g., in Populus, Pistacia, Salix, etc.). An intriguing recent study investigated the physiological traits of papaya seedlings with drought stress and well-water conditions (Trancoso et al., 2025). The results demonstrate that, based on physiological parameters (i.e., greenness index, combination of normalized difference vegetation index, photochemical reflectance index, water band index, simple ratio pigment index (SRPI) leaf number, leaf dry mass, and leaf mass ratio), under water-stress conditions, female and hermaphrodite seedlings can be separated, while in well-water conditions, SRPI and carotenoid reflectance index 2 distinguish female and hermaphrodite seedlings. This section presents a cross-taxa analysis in the context of physiological specialization as sex-specific strategy and response to stress. In addition, it also endeavors to draw generalizations across taxa and ecological contexts. With the current state of available studies, the unifying generalizations for the impact of abiotic factors on sexual dimorphism cannot be made, as also highlighted by Juvany and Munne-Bosch (2015), Retuerto et al. (2018), and Korres et al. (2023). This is due to species-specific results. Moreover, limited dioecious taxa have been investigated, which in turn restrict the chances of phylogenetic cross examination.

3.1 Does stress leads to sex-specific physiological specialization?

It is fairly apparent from the available studies that physiological specialization may not appear without stress. For example, in Amaranthus palmeri the sexes do not show any difference in total chlorophyll content grown under ambient, low, or even medium white light intensitie (Korres et al., 2023). However, high light intensity and nutrient deficiency leads to a greater leaf area and specific leaf area values in the male compared to female plants. Therefore, increase in chlorophyll content in the male plants at high light intensity were also observed. In Salix glauca, physiological specialization between the sexes was not present in water-availability conditions (Dudley and Galen, 2007). However, under drought/water stress conditions, sex-specific specialization as a physiological response becomes apparent—drought tolerance and gas exchange rates differ between sexes as males show lower stomatal conductance and transpiration rates than females. Even in Populus tomentosa, drought significantly affects photosynthetic efficiency, photosynthesis nitrogen-use efficiency, and stomatal conductance in both males and females, with values being lower in males, supporting their better physiological resource utilization (Lu et al., 2018). Likewise, in Urtica dioica, low temperature and water favor females, whereas high temperature alone leads to female mortality (Liu et al., 2021). These examples conform to the sex-specific plasticity of these traits, reflecting the high cost. This, in turn, suggests better physiological specialization in males for survival and as a sex-specific adaptive strategy.

Contrasting studies are available. For example, in Pistacia lentiscus under stress, water-use efficiency is higher in females in spite of lower photosynthetic rates, lower C assimilation rates, and lower values for stomatal conductance and transpiration than in males (Correia and Diaz Barradas, 2000). The study suggests that the physiological difference between sexes of the species is due to a different degree of stomatal variance rather than differences in photosynthetic activity, specific characteristics of the root system, and/or of xylem conduction. In addition, under factors such as salinity stress, contrasting results are available (see Section 1), indicating some extent of physiological specialization in dioecious taxa; deciding the direction of responses in cross taxa way will likely be unrealistic.

3.2 Does the combined effect of stress lead to sex-specific physiological specialization?

It is always proposed that the combined effect of multiple stressors may be much more pronounced than when each is acting independently (Chen et al., 2021). Populus cathayana is a good example: elevated C and temperature together increase water-use efficiency, photosynthetic N use, and leaf N content better in females than in males. However, at elevated temperature only, females show negative effects. This suggests that greater stress conditions increase female photosynthesis capacity, which enables their survival and reproduction. Interestingly, elevated C alone increases water-use efficiency, efficient photosynthetic N use, and N leaf content in males. Males exhibit greater C assimilation and adaptability in elevated C conditions. These results suggest that the interaction of these factors may modulate life-history strategies differently in dioecious taxa to achieve reproductive assurance (Chen et al., 2021) in a sex-specific manner (in females). Such interactions may also change the magnitude of physiological specialization between sexes in the species investigated. This may also be understood as an effort by females to meet the high cost of and ensure reproduction.

No clues were found in Ilex aquifolium for physiological differences between males and females, either at optimal light and water conditions (for water use efficiency, C to N ratio) or at limited water and light conditions (Retuerto et al., 2000). However, a combination of water availability and irradiance sex-specific responses were observed. In contrast to the abovementioned examples, in shade and xeric conditions together, I. aquifolium males utilized water more efficiently than females, suggesting that males use resources better under multiple stress conditions. Irrespective of treatment, females allocated higher N to leaves and maintained higher growth rates than male plants (Retuerto et al., 2000). It is tempting to again cite recent studies on I. paraguariensis that exhibit physiological differences between male and female plants, even in a vegetative state (Rakocevic et al., 2011, Rakocevic et al., 2023; Rakocevic et al., 2025). Such results within a genus suggest that physiological differences between sexes are context-dependent and species-specific (possibly clone-specific too). It could be postulated that high water-use efficiency and chlorophyll content in such species enable the survival of each sex, especially males in xeric conditions and perhaps females in stress conditions.

3.3 Harsh yet optimal conditions and no sex-specific physiological specialization

Plants growing in extreme environments are always means discovering more aspects of plants’ life sex-specific physiological specialization. The term “optimum conditions” should be applied with caution. Plants inhabiting extreme environment conditions often exhibit mechanisms that differ markedly from those documented in model or well investigated systems. In this context, studies highlight that even under harsh set of abiotic factors, physiological specialization may not emerge. For an instance, Liebig et al. (2001) investigated Clusia hilariana, a dioecious tree of coastal the restinga of Brazil, which grows in extreme conditions (high solar irradiance, high wind speed, elevated air and soil temperature). The leaf parameters like leaf fresh and dry weight, leaf area, and chlorophyll content do not vary between male and female trees. Chamaerops humilis is another example, which grows in Mediterranean-type ecosystems, which experience warm-dry summers and wet-mild winters. Mature plants of both the sexes are comprised of more carotenoid and other molecules to overcome stress (Morales et al., 2016). Even in Populus tremula, no confirmation of sexual dimorphism has been found in non-reproductive traits among male and female trees (Robinson et al., 2014; Melnikova et al., 2017).

3.4 Higher cost of reproduction in females and physiological specialization

Juvany and Munne-Bosch (2015) hypothesized that a higher cost of reproduction may reduce stress tolerance in females. In support of this, studies have reported poor vegetative, reproductive and physiological performance of females under stress conditions. Additionally, to fulfil their needs, females exhibit a C harvesting physiology that allows a greater production of vegetative mass (leaf area, number, higher C and N content) than males. Higher rates of photosynthesis in females correspond to water requirements. Hence, females prefer mesic sites. Males may invest in root growth, possibly to harvest nutrient from soil. Thus, male have the capacity to survive in xeric environments. Species such as Leucadendron sp. have shown higher specific leaf area and higher N content for females than males, supporting the idea of a higher cost of reproduction and to maximization of reproductive efforts by females (Midgley, 2010). As highlighted in the context of sex-specific water requirements in available studies, it can be ascertained that males may tolerate adverse conditions better than females. These habitat preferences suggest a dimorphism in physiological traits associated with cost of reproduction.

3.5 Stage of the evolution of dioecy and sex-specific physiological specialization

The stage of the evolution of dioecy may also limit the impact of abiotic factors on it and physiological specialization. For example, studies on the cryptic dioecious Thalictrum pubescens have established that no significant differences exist between the sexes for vegetative and reproductive traits, including in context of abiotic factors—availability of light, nutrients and soil moisture—and in the nutrient concentrations of tissues. No incidence of intersexual competition was evident in female or male growth; thus, there is no impact on the spatial segregation of the ramets of the species. The distribution of ramets/genets in overlapping habitats indicate that males are not better competitors than females, which is a generalization regarding dioecious plants (Timerman and Barrett, 2019). Likewise, in sub-dioecious Corema album (Empetraceae), the female invests three times more biomass in vegetative and reproductive structures than males and hermaphrodites, which can be attributed to higher resource investment required by females for fruit set (Zunzunegui et al., 2006). However, physiological specialization was obscure, as photosynthetic rates and water use efficiency do not vary between males, females, and hermaphrodites.

Among gynodioecious taxa such as Schiedea salicaria and Lobelia siphilitica, females and hermaphrodites only differed in photosynthetic efficiency, and specific leaf area is higher in females; in Schiedea adamantis, Sidalcea hirtipes, and Plantago lanceolata, this is not so. There is no variation in water use efficiency between sexes except in P. lanceolata. Even other vegetative and reproductive traits exhibited limited/no sex-based differences (Poot et al., 1996; Caruso et al., 2003; Schultz, 2003; Culley et al., 2006). Studies clearly demonstrate that the extent of sexual dimorphism as physiological specialization is species specific and that the absence of sexual dimorphism in physiological traits is largely due to early stages of evolution of dioecy prevailing in species such as S. adamantis.

4 Role of competition: a preliminary analysis

Research has extrapolated the effect of abiotic factors in addition to intersexual and intrasexual level competition (Hesse and Pannell, 2011; Barrett and Hough, 2013; Tonnabel et al., 2017). Thus, competition emerges as an imperative factor to be concisely considered in the present review, although it is a biotic component of ecology. Degree of competition may modulate the consequences of abiotic factors on dioecious taxa and show the modular adaptability of a sex or between sexes. Intersexual competition interactively affects growth, photosynthetic capacity, and biomass in Populus sp. (Chen et al., 2014; Chen et al., 2017; Chen et al., 2021). These consequences may be interactive between the factors and sexes as highlighted previously. For example, male Lithraea molleoide s plants under drought may outcompete females (due to supportive resource allocation pattern and physiological differentiation), thus having better survival adaptability than females. This corroborates the idea of better intersexual competitive strategies among males than females. Under light-limiting conditions and intersexual competition, females exhibit more plasticity towards reproductive allocation and trade-off for vegetative allocation, such an in Mercurialis annua (Tonnabel et al., 2017; Galfrascoli and Calviño, 2020). In general, these strategies reiterate attempts by females for successful reproduction.

Density may also affect the degree of competition for resources and resource allocation strategies in males and females. Higher density does not have a significant effect on vegetative traits in both males and females of M. annua, but the relative reproductive allocation and reproductive efforts of females is reduced (Tonnabel et al., 2017). The greater trade-off in females reflects a strategy of maximizing current reproductive success in terms of C acquisition and seed maturation at higher densities and light-limiting environments (Tonnabel et al., 2017). Research suggests that females are better competitors than males in the context of inter-sexual competition that arise due to reliance on similar resources in overlapping niches. Herrera (1988) observed that sex specific competition in Osyris quadripartita is asymmetrical and that males are inhibited by competing with neighboring females. Sánchez Vilas and Pannell (2011) found that both intra- and inter-sexual competition affect the aboveground growth of males but not the growth of females in M. annua. Male and female Populus cathayana show different responses in context of inter- and intra-sexual competition (Chen et al., 2017; Melnikova et al., 2017). Females show higher growth rates and outcompete male seedlings. Higher biomass accumulation is seen in females in intersexual competition treatments compared to males than in intrasexual competition. These results suggest that in inter- and intra-sexual competition, female performance is higher in terms of biomass allocation and physiological parameters (e.g., photosynthesis capacity) despite the woody or herbaceous nature of species. It could be postulated that in dioecious taxa, competitive ability is reflected in physiology, resource allocation, and other life-history strategies to specifically provide reproductive assurance.

The balanced or skewed sex ratio among dioecious taxa could be associated with abiotic and biotic factors such as pollination, growth form, clonality, cost of reproduction, and resource availability (Barrett, 2015). However, the ratio could also rely on the innate life-history traits of species in context: differences in the competitive ability of the genders, sex-specific mortality (based on age or size), and the spatial segregation of sexes (resource-rich or -poor areas) (Field et al., 2013a; Field et al., 2013b). Life-history strategies such as wind pollination may also impact competitive ability between sexes. For example, environmental factors (wind, temperature, water, etc.) affect males more severely than females in Rumex lunaria. At higher altitudes, higher male mortality was observed and contrastingly, female plants were higher than male plants (Bürli et al., 2022). Research on annual and perennial species reveal different extents and consequences of both inter- and intrasexual competition and survival. In a climate change scenario, studies are revealing the facilitative shift in root growth in mixed-sex plantings and the synergistically increase in whole-plant nutrient pools (Korres et al., 2023). While detailed examination is beyond the scope of this review, the competitive behavior of dioecious taxa must be recognized when planning agroforestry systems, weed management, orchard establishments, and related practices.

5 Conclusions and future prospectus

Sexual dimorphism in plants manifests at various levels, including sex-specific physiological specialization (Figure 1), yet its extent is quite species-specific, making any generalization unsuitable (Table 1). Nonetheless, the lack of any generalization highlights the crucial role of species-level studies for more insights. The pertinent studies have not emphasized underground structures such as roots, runners, and suckers in relation to plant habits (shrub, herb and trees), which are key to survival. There is an important lacuna in the context of evolutionary strata and abiotic factors in shaping sexual dimorphism. The limited available of studies proposing the absence of sexual dimorphism in physiological traits is mainly due to the early stages of the evolution of dioecy. However, this hypothesis is yet to be tested, and generalizations cannot be made.

TABLE 1. Abiotic factor and its effect on sexual dimorphism and ecological correlates of dioecy. These effects highlight the eco-evolutionary significance of interaction between abiotic factor and sexes in dioecious taxa. However, these are context-dependent, and broad generalization is limited.

In context of trait plasticity exhibited by the sexes in response to abiotic factors, it is essential to distinguish plastic responses from underlying genetic variations, as highlighted by Puixeu et al. (2019) on Mercurialis annua. Despite this recognition, further research remains necessary. The role of sex chromosomes has been proposed for maintaining sexual dimorphism (Charlesworth, 2018); however, genetic and molecular bases of resource allocation in relation to abiotic factors have not been investigated in much detail. The concept of “optimal ecological conditions” should always be a species-specific consideration. With stress conditions, species growing in extreme habitat conditions may serve as a classic system for comparative analysis. While numerous experimental studies have been conducted, anatomical and ultrastructural studies have been largely neglected. Such studies may highlight the sexual dimorphism and sex-specific strategies in a more detailed way.

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Footnotes

Edited by: Weverton Pereira Rodrigues, Universidade Estadual da Região Tocantina do Maranhão (UEMASUL), Brazil

Reviewed by: Miroslava Rakocevic, State University of Northern Rio de Janeiro, Brazil

Zhi LI, Henan Agricultural University, China