Why Olive Produces Many More Flowers than Fruit—A Critical Analysis

Abstract

Olive (Olea europaea L.) trees produce many more flowers than fruit. In an “on” year, an adult olive tree may produce as many as 500,000 flowers, but 98% of them will drop soon after bloom as unfertilized flowers or juvenile fruit. This waste of resources that could be better invested in fruit reaching maturation requires an explanation. Several, not mutually exclusive, hypotheses explaining the possible significance of heavy flowering followed by massive and premature flower and fruit abscission are analyzed and compared based on previously published works and recent observations on olive reproductive biology. The results suggest that olive trees selectively abort fruits to enhance the quality of the seeds in the surviving fruits. Additionally, a considerable proportion of flowers appears to contribute to the male fitness of the plant by increasing pollen export. Conversely, the hypotheses attributing to resource limitation, pollination deficits, pollinator attraction, or extra flowers functioning as an ovary reserve, must be rejected for explaining the ultimate functions of massive flower production. Implications for olive orchard management are discussed.

1. Introduction

Many plant species regularly abort a large portion of their flowers and juvenile fruits that could otherwise develop to maturity. The overproduction of flowers that do not reach maturation is a widespread feature among many Angiosperms, but it is especially common and particularly pronounced in woody, outcrossed, hermaphrodite plants [1,2], including many fruit crops. In these species, surplus flowers and fruit are abscised early. This drop of juvenile fruit is known in pomology as “June drop” because, in the Northern Hemisphere, most fruitlet abortion in apple, and in other temperate fruit crops, mostly occur in June. This waste of energy is surprising, as it seems that the resources invested in surplus flowers and aborting fruitlets could be better allocated to increasing the number and size of fruit that reach maturation [3,4]. For this reason, significant effort has been devoted to determining the causes and significance of this massive flower and fruit abortion in cultivated fruit trees, as well as in wild species. In this context, several hypotheses aim to explain the benefits of producing these massive numbers of flowers. Since the cost of over-initiating flowers and fruit is substantial [5], the benefits of their formation must outweigh the expenditures incurred, in order to reasonably explain why this trait has been fixed and widespread during the evolution of flowering plants.

In olive, different research teams have explored the mechanisms underlying massive flower and fruit abscission, aiming to suggest crop management practices that might increase the low fruit set characteristic of this crop. An olive tree may produce as many as 500,000 flowers in its “on” year, but only 1–2% of them reach harvest as ripened fruit [6]. The remaining 98–99% abscise as flowers or young fruit, mostly within the first two months after bloom [7]. In this study, I critically analyze current hypotheses formulated in the literature to explain the significance of premature flower and fruit abscission in domesticated and wild species to check its appropriateness to explain the olive massive flowering and low flower/fruit ratio. These hypotheses are evaluated using results from previous published investigations, as well as new knowledge about the reproductive biology of Olea europaea. The aim of this work is to determine the ultimate reasons why olive trees produce many more flowers than fruit. Stephenson [1], in his seminal review on this topic, distinguished between proximate causes, as the mechanisms responsible for the failure of flowers to set fruit, from the ultimate reasons, referring to the functions that surplus flowers that consistently fail to reach maturation may play in the reproduction of these plants. This distinction is particularly pertinent to the objectives of this review.

2. The Plant

The domesticated olive tree (Olea europaea subsp. europaea L.) is a woody wind-pollinated, preferentially allogamous crop of immense importance in the Mediterranean region. Its longevity and historical significance have attained the status of myth in several monotheistic religions of the Mediterranean, being, frequently mentioned in the sacred texts of Christianity, Judaism, and Islam. The olive tree is andromonoecious, producing both hermaphrodite and staminate flowers in panicles of between 15 and 30 flowers on average, depending on the cultivar and growing conditions [8]. The panicles develop in high numbers (often more than twenty), clustered in the axil of leaves on 1-year-old shoots (Figure 1).

Olive panicles are ramified and, in addition to the apical flower (“king flower”), they have primary, secondary, and, occasionally, tertiary branches [9]. Hermaphrodite flowers are mostly located on primary branches, while staminate flowers are more frequent on secondary and higher order branches [10,11] (Figure 2).

The olive tree exhibits a strong alternative bearing habit, with “on” years of massive flowering followed by “off” years with few or no flowers. In its “on” year, an adult olive tree blooms profusely, producing as many as 500,000 flowers [6]. However, not all these flowers reach harvest because up to 98–99% of them drop, either as flowers or developing fruitlets, within the first two months following bloom [7]. Three main waves of abscission can be distinguished in olive. The first wave affects staminate flowers, which drop a few days after bloom, once they have accomplished their mission of exporting their pollen grains [10]. The second wave impacts unfertilized, yet fertile, hermaphrodite flowers, which drop in the second week after bloom. Despite the magnitude of these two phases of flower drop, the olive tree still initially set a much larger proportion of fruit than those ultimately reaching harvest. Thus, after fertilization of the flowers, many developing fruitlets begin to grow, triggering an intense fruitlet competition resolved with the abscission of many of them. This process stabilizes the fruit population after the third wave of fruitlet abscission, occurring five to seven weeks after flowering [12,13]. This final drop wave may partially overlap with the abscission of unfertilized flowers [14]. Regardless of the reasons behind the failure of flowers and fruit to reach maturity, sound explanations are required for explaining the formation of such a large number of flowers and the over-initiation of fruit that will ultimately abscise. Below, I explore several current hypotheses trying to explain the benefits of producing this extraordinary number of surplus flowers in olive.

3. Hypotheses to Explain Massive Fruitlet Abortion

Six valid, not mutually exclusive, hypotheses attempt to explain the massive flower and fruitlet abscission observed in many hermaphroditic angiosperms. The hypotheses explaining the production of surplus flowers are: (1) pollinator attraction, where flowers serve to attract a greater number of biotic pollination vectors; (2) abscission due to pollination deficits, either from the scarcity or the inadequacy of the pollen grains landing on the stigma, or because pollinators fail to visit all the flowers; (3) excess flowers serving solely a male function, exporting their pollen grains and thus enhancing male and, consequently, the total fitness of the progenitor plant; (4) flower drop caused by resource or nutrient limitations, including here water deficits; (5) the bet-hedging hypothesis, which suggests that there are no surplus flowers, but rather that they are formed in case unexpectedly favorable seasons might allow a full fruit set; and (6) sexual selection and selective abortion among developing fruitlets based on fruit and seed sink strength (genotype based).

The validity of these hypotheses in explaining massive flower and fruitlet abscission in olive is evaluated based on both my own research and previously published studies by other colleagues on olive reproductive biology. These findings are critically analyzed to determine the ultimate reasons behind the production of surplus flowers in olive.

3.1. Pollinator Attraction

The first hypothesis postulates that an excess number of flowers are formed, especially when bloom occurs in inflorescences [15] to attract biotic pollinating agents (pollinators) more effectively by offering floral rewards at a lower cost. In this regard, the basic unit of attraction for pollinators is the inflorescence. However, olive is wind-pollinated. Indeed, olive belong to the Oleaceae family where many species are insect-pollinated species, and olive flowers still possess a conspicuous white corolla and emit a sweet aroma that attracts insects, primarily honeybees [9]. This ambophily has been identified in the closely related species Olea ferruginea [16]. Nonetheless, it is evident that olive has evolved toward anemophily, and during an “on” year, adult plants produce billions of pollen grains (approximately 50,000 million pollen grains per tree, extrapolating data from Cuevas and Polito [10] and Rojas-Gómez et al. [17]). This pollen is readily transported by the wind, as evidenced by the seasonal allergies experienced by many people in Mediterranean countries (Figure 3).

Although a ancient function of surplus flowers attracting insects cannot be entirely dismissed, if this were their primary role in olive, then a large number of flowers formed during “on” years would result in greater pollinator attraction and, consequently, in a proportionally higher reproductive success [18]. However, olive trees with more flowers set proportionally fewer fruits (Figure 4). On the contrary, trees in their “off” year set proportionally more fruits on average [19]. Consequently, surplus flowers do not function to attract pollinators in olive.

3.2. Pollination Deficits

A different hypothesis suggests that fruit set is limited by pollination deficits. These deficits can be due to a shortage or inadequacy of the pollen grains or from the absence of pollinators [20,21]. As stated earlier, olive is wind-pollinated, and a single adult tree can produce billions of pollen grains. Although wind is a random pollination vector, many field experiments have shown that most, if not all, hermaphrodite flowers receive enough pollen grains on their stigmas to achieve fertilization. This has been demonstrated in multiple studies where pollen loads on stigmas were quantified in flowers left exposed under conditions of open free-pollination [22,23,24,25,26,27]. Cases of pollen scarcity on stigmas have been rarely documented [13], and when observed, they likely reflect the late abortion of a small portion of flowers with non-functional stigmas (Figure 5D) rather than a problem with pollen transport.

An alternative approach here is to suggest that it is not the quantity, but the quality of the pollen that might lead to a lack of fertilization and, consequently, to flower abscission in olive orchards. Self-incompatibility in olive has recently been confirmed to be of the sporophytic type and is known to severely affect many olive cultivars [28,29]. While olive has repeatedly been acknowledged as a self-incompatible species [22,28,29,30], massive flower and fruitlet abscission still occurs even under optimal cross-pollination conditions. In fact, highly successful fertilization achieved by cross-pollen anticipates fruitlet abscission, as earlier and higher levels of flower fertilization promote earlier fruitlet growth that triggers the abscission of less competitive fruitlets [13].

Fertilization levels of 40–50% of the hermaphrodite flowers have been reported for different olive cultivars under cross-pollination conditions [22,23,31,32]. Furthermore, Rapoport and Rallo [7] found that more than 50% of the abscised pistils of Manzanillo (syn. Manzanilla de Sevilla) cultivar were fertilized, ruling out pollination deficits as a cause of their drop. Unfortunately, high fertilization rates in olive do not guarantee similar high levels of final fruit set. Even under the best conditions, fruit set does not exceed 10% of the hermaphrodite flowers produced [13,22]. Certainly, the benefits of cross-pollination are undeniable, as it significantly increases fruit set and yield in olive orchards [31,33,34,35]. However, pollination deficits, either in quantity or quality, are insufficient to explain the cost of producing significantly more flowers than fruits in olive. Therefore, although cross-pollination markedly enhances fruit set in most cultivars, and although some level of pollination deficits might appear in large monovarietal orchards due to the strong olive self-incompatibility, even under those optimal pollination conditions, massive June drop persists. Therefore, the pollination deficits theory does not adequately explain the surplus flower production in cultivated olive.

3.3. Male Function

This hypothesis posits that surplus flowers that later drop are in fact accomplishing only a male function; that is, they serve for exporting their pollen grains to achieve fertilization in flowers of other plants [36,37,38,39]. In other words, according to this theory, despite being morphologically hermaphrodite, most or all abscised flowers are, in fact, functionally male, and the surplus flower production is explained by enhancing the male competition component of sexual selection [40]. Extensive analyses across numerous species have shown that pistillate flower abortion rates are lower in monoecious and dioecious plants compared to hermaphrodite plants [2]. This pattern is explained because monoecious and dioecious plants can separate better the investments in male and female organs, adjusting therefore more tightly the resource allocation for pistillate flowers to those more likely to reach ripening. If this were the case for olive, it is not easily understandable why olive has not transitioned to monoecy to form some of the flowers just as staminate, saving resources otherwise spent on surplus pistil formation. In hermaphrodite plants, reproductive resource allocation is divided between male (pollen) and female (fruit and seeds) organs [1,41], with the latter being significantly costlier to produce. Evolution towards monoecy or dioecy would allow plants to allocate resources more strategically based on environmental constraints and available resources. However, in olive, andromonoecy appears to be a fixed trait [10], and the overproduction of hermaphrodite flowers in excess cannot be fully explained by the male function hypothesis. Additionally, the production of an important number of fruitlets that later abscise during the June drop period also denies the notion that these flowers were formed solely to accomplish the male function by exporting their pollen grains.

Staminate flowers in olive result from pistil abortion (Figure 5B,D). Pistil abortion can occur at various stages of flower development, but in most cases, pistil growth is arrested early, leading to flowers that either lack pistils or have rudimentary ones [42,43]. In some cases, however, pistil formation progresses almost to completion, although the stigma papillae fail to develop fully (Figure 5D), so the flowers are not able to adhere pollen grains and, as a result, they are unable to set fruit [43]. The occurrence of pistil abortion at different developmental stages suggests that olive trees are continuously balancing the amount of the available resources [44], including water, to invest in pistil development with suboptimal conditions leading to higher rates of pistil abortion. In this regard, the production of staminate flowers is extremely variable among cultivars, years, trees, branches and even among panicles on the same shoot. However, it tends to increase during dry seasons and under nutritional deficiencies [42,44].

Figure 5. Scanning electron microscopy images of hermaphrodite (left) and staminate (right) olive flowers. (A). Detail of a well-developed stigma (SG) adjacent to one stamen (ST). (B). Pistil-aborted flower showing a rudimentary pistil (PI). (C). Pollen germination on fully developed stigma papillae. (D). Functionally male, late pistil-aborted flower displaying stigma with non-functional papillae. Source: own author [42].

Figure 5. Scanning electron microscopy images of hermaphrodite (left) and staminate (right) olive flowers. (A). Detail of a well-developed stigma (SG) adjacent to one stamen (ST). (B). Pistil-aborted flower showing a rudimentary pistil (PI). (C). Pollen germination on fully developed stigma papillae. (D). Functionally male, late pistil-aborted flower displaying stigma with non-functional papillae. Source: own author [42].

Staminate flowers also formed in less favorable sites within panicles, suggesting again resource limitation as the cause of their formation. Their selective placement on poorly nurtured sites, such as secondary and tertiary branches of the panicle [10,11] (Figure 2), underscores the role of resource competition. This architectural negative effect on their fate reinforces the idea that competition for resources plays a role in their formation [11,44]. Plant architecture, particularly pedicel thickness, is closely associated with critical components of female reproductive success, including fruit and seed set, seed number, and size [45,46]. In an apparent contradiction, the resources saved by not developing a pistil in the staminate flowers of olive are not allocated to other organs within the same flower. This is evidenced by the smaller size of petals and sepals of staminate flower compared to hermaphrodite ones [10]. Nonetheless, compared to hermaphrodite flowers, the staminate flowers produce an equal number of pollen grains per anther, pollen grains that are of the same size and viability, and with the same capacity to perform ovule fertilization in hermaphrodite flowers of other cultivars [10]. These findings indicate that staminate flowers enhance male and, consequently, total plant fitness at a lower cost, since the staminate flowers can sire the same number of embryos in other plants than the hermaphrodite flowers while being less costly to produce [10,47].

Consequently, an important proportion of olive flowers are staminate and hence do not have the capacity to develop into fruit. Their effective achievement of the male function explains the formation of those staminate flowers, but this cannot explain why many extra hermaphrodite flowers are still formed.

3.4. Resource Limitation

If the formation of staminate flowers in olive is at least partially attributable to resource limitation, we may think that, perhaps, the reduced fruit set in hermaphrodite flowers is also due to the lack of resources, being this lack of resources circumstantial rather than structural [48,49]. According to this hypothesis, under certain conditions, all or most hermaphrodite flowers could potentially mature into fruit. However, fruit set in olive is always very low, and there is no significant seasonal or spatial (orchard) variation allowing all flowers to reach ripening. While proper orchard management practices, particularly irrigation and fertilization, can modestly increase fruit set in olive, unfortunately improvements are limited at the most to 5–6% of the flowers formed [5].

It is clear, however, that competition for resources among developing fruitlets is the proximate cause, the mechanism, triggering the intensive post-anthesis fruitlet abscission in olive. This competition occurs initially among fruitlet within the same panicle and later between fruit on neighboring panicles [11]. This conclusion is supported by results of different thinning experiments and by the observation that early fruit growth immediately precedes the abscission of both fertilized and unfertilized flowers [13,14]. In this regard, thinning experiments have demonstrated that removing more than 50% of panicles increases the fruit set of the remaining flowers without reducing the final number of fruit at harvest [50]. This result confirms the surplus nature of many flowers, with up to 60% deemed excessive in certain experiments. Similar findings are obtained when entire inflorescences are removed or when selective thinning is applied by eliminating some flowers within a panicle. Notably, the result remains consistent regardless of whether flower removal is performed before or during the first days after bloom [12,50,51].

It is worth noting that small-fruited cultivars exhibit higher fruit set than large-fruited cultivars [47], although overall productivity per tree does not differ significantly. Additionally, small-fruited cultivars have smaller ovaries at bloom compared to large-fruited cultivars [52,53], so they are less competitive, or less “selfish” we might say. Similar results were observed in experiments with ‘Galego’ olive trees grown in pots under low temperatures (20/14 °C). At these low temperatures, reduced fruit growth rates decrease fruitlet competition and allowed fruit set to double compared to trees grown at 25/20 °C, although the final fruit size at harvest halved under the lower temperatures [54]. Cool springs also have a positive effect on olive fruit set, likely by reducing fruit growth rate and, therefore, fruitlet competition by resources.

Thus, while good orchard management can and should increase fruit set and yield in olive orchards, it will never do so to the extent of completely avoiding fruitlet drop. On the other hand, flower thinning experiments confirm that competition for resources is the proximate cause of the abscission of fruitlets, but not the ultimate reason for the formation of so many flowers in olive. Therefore, an alternative explanation for the production of surplus hermaphrodite flowers remains necessary.

3.5. Bet Hedging-Ovary Reserve Hypothesis

The bet hedging hypothesis shares some common ground with resource limitation theory, as it also justifies the formation of extra flowers to maximize fruit set during favorable seasons. According to the bet hedging hypothesis, surplus flowers are produced to exploit unexpected prodigious seasons with abundant resources (for wild Olea europaea, we will say rain) [1,55], allowing full fruit set in favorable environments. However, in domesticated olive, there is neither spatial nor temporal variation in fruit set that allow all fruit to complete maturation. As mentioned before, this holds true under optimal orchard management or in exceptionally favorable years. Moreover, the fact that many olive flowers drop after fertilization and at various stages of embryo development [14] further suggests that olive trees cannot develop all the hermaphrodite flowers they produce, making it unrealistic to expect all of them to reach maturity. On the other hand, the activity of pollinating insects plays no significant role in olive reproduction, as olive is predominantly wind-pollinated. Therefore, the idea that optimal pollination in exceptional seasons might justify the production of surplus flowers is not a suitable explanation for olive massive flower production. Consequently, bet hedging hypothesis fails to justify the formation of surplus hermaphrodite flowers in cultivated olive trees.

A variant of bet hedging theory, the ovary reserve hypothesis, posits that many flowers are produced to counteract unpredictable, externally induced mortality that is not maternally regulated [56], especially, but not only, herbivory [4]. According to this hypothesis, surplus flowers serve as an insurance against flower losses [57], or even as a bait for herbivores, achieving seed predators’ satiation by producing more flowers (and seeds) than necessary [48,55]. If this were the case, the sacrifice of some pistils for the benefit of others would take place throughout the entire reproductive season, providing protection to sibling fruits from seed predators from bloom to fruit maturation and seed dispersal. However, in olive, most juvenile fruit drop occurs very early in the season, leaving sibling fruits exposed to predators for the majority of the reproductive period. It remains possible that the plant’s strategy is to safeguard the bloom period, with resource competition among fruitlets driving the abscission of weaker juvenile fruits thereafter. Ehrlen [56] proposed that the number of surplus flowers increases with increasing fruit-cost/flower-cost ratio and ovary mortality. As a result, species with costly fruit and small flowers, such as olive, would exhibit higher rates of fruit abortion.

Guitián et al. [58] found that when flower mortality is high in Cornus sanguinea, subsequent fruit abortion is reduced, suggesting that, in this species, surplus flowers act, at least partially, as an insurance against flower predators. A similar conclusion was reached for Prunus mahaleb [59]. Certainly, in olive, larvae of certain pests, such as the second generation of Prays oleae, prey on hermaphrodite flowers (eating the ovary), while the third generation damages small fruitlets. However, the extent of this predation seems not sufficient to pose a significant threat to olive fruit production. On the other hand, if ovary reserve hypothesis were applicable to olive, we would expect substantial seasonal variations in fruit set depending on herbivory incidence. However, fruit set in olive consistently remains low, and massive flower and fruitlet abscission occurs even in the absence of pest damage. We could argue that domestic olive cultivation protects the crop against extensive pest damage, but this is not always the case. Furthermore, wild olives (Olea europaea subsp. sylvestris) and close relatives, such as Olea europaea subsp. cuspidata, are not subjected to farmer protection against pests, and they also produce few fruits per panicle and exhibit similar levels of flower and fruitlet abscission [60,61].

Thus, the conclusion is that surplus flowers are indeed formed in olive, and that their elimination, whether by herbivores, by thinning, or pruning, is partially compensated by increasing fruit set among the survival flowers. However, this compensation does not suffice to achieve a full fruit set. Consequently, circumstantial high levels of herbivory do not justify the significant expenditure incurred by olive trees in producing up to fifty times more flowers than the number of fruit that reach harvest.

3.6. Sexual Selection, Sibling Competition and Selective Abortion

Previous hypotheses fail to explain fully the ultimate reasons for, and the significance of, surplus flower production and massive fruit abortion in olive. One last hypothesis suggests that olive produces more flowers and fruit than needed to facilitate the selection of the best of them based on the quality of the next generation (“the survival of the fittest”; [62]). Selective abortion has been documented in many species with multi-seeded fruits. In such species, maternal investment in fruit development is maximized by aborting fruit with fewer or weaker seeds [1,63,64]. In olive, which produce drupes, selective fruit abortion is primarily determined by the size and strength of the single seed that typically forms within the endocarp. Drupes rarely contain more than one seed, although some olive cultivars show a tendency to produce bi-seeded fruits, especially under cross-pollination conditions [65]. Since the endocarp functions as the dispersal unit, the presence of two seeds within a single stone is detrimental for the size of each individual seed [65], and likely reduces seedlings survival in nature due to intensified sibling competition in the same ground site after endocarp dispersal by birds.

It is plausible that mother olive trees produce extra flowers and fruitlets for letting many of them drop. As discussed earlier, this is not a behavior exclusive to olive trees; as many woody plants, including other fruit crops, produce significantly more flowers than fruits [1]. The right question itself extends to why many plants produce many more ovules than seeds [66], considering that seeds represent the next generation of sporophytes, with fruits serving as dispersal vehicles for seeds. Regardless of how the question is framed, one plausible answer is that olive form surplus flowers and ovules to enable the selection of the fittest seedlings, promoting the abortion of weaker fruitlets and the selection of the best embryos. Lee [67] elegantly developed the gametophyte competition theory, proposing that plants selectively mature fruits from ovaries where pollen tube competition has been most intense. He hypothesized that the embryos resulting from the fertilization of ovules by faster-growing pollen tubes would produce sporophytes with higher fitness. Resource limitation and differences in the quality of pollen achieving fertilization will thus open the possibility for sexual selection during fruit development [63]. Experimental evidence supporting the theory of selective abortion, sexual selection, and sibling competition and how it operates in olive is presented below.

4. How Sexual Selection Operates in Olive

Olive trees appear to select the best embryos through a series of mechanisms: selecting the fastest pollen tubes (carrying the male gametes), the most attractive ovules (enclosing the embryo sac with the egg cell and polar nuclei) for double fertilization, and the strongest siblings after fertilization. The first step of sexual selection occurs in the transmitting tissue of the recipient pistil. A single olive pistil may receive over 1000 pollen grains on its stigma [26,68], many of which germinate and grow forming pollen tubes carrying the male gametes at their tips. The initial selection of the male gametes is based on the adequacy of the genotype of the pollen grain, since most olive cultivars are predominantly allogamous and discriminate against self-pollen through self-incompatibility reactions [28,29,30]. Nevertheless, under open- and cross-pollination conditions, dozens of pollen tubes often grow within the transmitting tissue of the pistil, although usually only one pollen tube reaches the base of the style to enter the ovary [22,33,68,69] (Figure 6). Intense pollen tube growth attrition ensures that only the fastest pollen tube access the ovary, where now, the “winner” fastest pollen tube encounters four viable ovules.

Intense competition within the transmitting tissue of the pistil is not limited to the male gametes; female gametes contained in the ovules may also be subjected to selective pressures, since only one of the four ovules of the ovary will normally become the seed. This raises an important question: Why do olive flowers contain four ovules when only one typically develops into a seed? In olive, the four ovules are equally sized at bloom, occupy symmetric positions within the ovary, and do not seem to differ in fertility or longevity. Secondary ovules exist in the flowers of stone fruit crops, where secondary ovules usually lag in development, being the primary ovule normally the only one fertilized. However, in olive, there are no obvious reasons why the selected pollen tube would choose one ovule over another. Nevertheless, this selection process is unlikely to be random. Cuevas et al. [68] proposed that this scenario enables ovule competition for the sole pollen tube accessing the ovary, representing a rare case of female competition and male choice in flowering plants.

Upon exiting the transmitting tissue, the pollen tube responds to attractant signals from the ovules, growing along the funiculus surface and entering the ovule’s micropyle to perform double fertilization, a process exclusive to angiosperms. In this regard, we know that synergids cells play a crucial role in attracting the pollen tube to the filiform apparatus [70,71]. Calcium ions (Ca²⁺) serve as critical signaling elements for pollen tube guidance and fertilization. As the pollen tube nears the filiform apparatus, attractants secreted by the synergid cells modulate Ca²⁺ concentration at the pollen tube tip, facilitating the interaction between the pollen tube and the receiving synergid cell [72]. The synergid cells also provide resources in this last step of pollen tube growth, culminating in the discharge of two male gametes into the embryo sac [70,73]. A differential capacity of the synergid cells of different ovules to attract the pollen tube might explain in olive the preference of the “winner” pollen tube for a specific ovule. This, along with the formation of four ovules per flower could represent the first reported case of ovule (female) selection and male choice in flowering plants [68], even though this circumstance may be present in many other multi-ovulated ovaries sharing the same characteristics of olive flowers, and producing single-seeded fruit. It is noteworthy that the genes of synergid cells are not transmitted to the next generation, unlike the genes of the egg cell after double fertilization. Thus, the role of the synergids, sisters to the egg cell, may represent a unique example of altruism.

If the strong selection of male and female gametes were not enough, olive trees further promote sibling competition after fertilization by displaying numerous flowers together in a single panicle. This arrangement intensifies competition for limited resources, first within the panicle and then among developing fruit on nearby panicles [12]. Large inflorescences and simultaneous flower opening reinforce effective sexual selection and sibling competition by favoring the abortion of weaker fruitlets that grow at a lower rate [36]. Similar observations have been reported in Prunus mahaleb, where the inflorescence also functions as the fructification unit [59]. In this context, fruitlet abscission primarily affects the smaller fruitlets, which may result either from delayed fertilization achieved by a slower pollen tube or from weaker seeds that grow more slowly. Both factors reduce the competitiveness of these fruitlets for survival, leading ultimately to their drop. In olive, it is still unclear which flowers are more likely to become fruit, whether those with pistils fertilized first or those that grow faster [13]. In contrast, Hiei and Ohara [74] observed in Melampyrum roseum that flower better positioned in the inflorescence and those that open earlier exhibit higher fruit set. Medrano et al. [75] suggest that resource sequestration by the earliest developing fruit in Pancratium maritimum is also the cause of the abscission of the smaller fruitlets.

Simultaneous and massive full bloom is a prerequisite for making sexual selection more effective, as scattered flowering diminishes sibling competition and sexual selection opportunities. In olive, there are only slight phenological differences within a panicle and among nearby panicles, with bloom mostly occurring simultaneously. In some species, it has been shown that the percentage of fruitlets resulting from self-fertilization decreases during the fruitlet abscission period, as maternal plants preferentially select fruitlets produced through cross-fertilization [1]. In avocado, this selection favoring stronger seeds leads to the production of larger fruit, which benefits farmers economically [76,77]. In olive, demonstrating this phenomenon presents challenges due to the difficulty extracting DNA from abscised fruitlets and dead seeds. Sexual selection in domesticated olive might somehow benefit table olive farmers, as studies have shown that, in olive, seed weight is linearly related to fruit weight, reflecting seed’s sink strength in attracting photo assimilates for fruit growth [65]. Seed size, in turn, is related to seedling survival and might be a critical factor in harsh Mediterranean environments. Ultimately, the goal of this strong selection among seedlings in wild olives is to produce seeds of superior quality capable of surviving after germination in an environment characterized by prolonged drought and nutrient-poor soils.

5. Implications for Olive Cultivation, Future Prospects

The consequences of strong seedling selection extends to different aspects of orchard management in domestic olive. In this regard, farmers must understand that massive flower and fruitlet abscission are inherent to the reproductive system of the olive tree and cannot be eliminated by increasing fertilization or by over-irrigation. The lack of resources is not the ultimate reason why olive produce so many flowers and regularly abort many fruit. Certainly, flower thinning in olive can increase fruit/flower ratio, but it does not raise the number of fruits per panicle. Therefore, surplus flower production is not explained by resource limitation, although the competition for resources is the mechanism through which olive selectively abort less competitive fruitlets. On the contrary, these extra flowers are primarily formed to facilitate the selection of the best embryos by means of the selective abortion of the weaker fruitlets. Therefore, neither irrigation, despite being a key factor for olive production, nor heavy orchard fertilization can prevent fruitlet competition and drop. However, these management practices wisely carried out can enhance available resources, increasing thus fruit set and the proportion of flowers that reach harvest.

Flower thinning and pruning reduce the flowers population, thereby lowering fruitlet competition. However, as competition starts within the panicle and later extends to nearby panicles, these techniques cannot completely eliminate fruitlet abscission in olive. The fact that fruit load at harvest remains unchanged after removing a large proportion of flowers at bloom indicates that fruit set is proportionally increased by reducing the population of flowers. Nonetheless, heavy flowering during an “on” year usually leads to high yields, which in turn inhibit flower induction for the following season [78], resulting in a reduced crop during the “off” year, a characteristic behavior of alternate-bearing cultivars. This suggests that selecting cultivars with lower flowering levels could minimize the wastage of resources due to heavy flowering and, at the same time, reduce olive alternate bearing habit [5,6]. Such selection should focus on genotypes with fewer flower per panicle and panicles uniformly distributed around the canopy to minimize fruitlets competition. In this context, chemical fruit thinning in olive oil cultivars warrants some more research. As previously mentioned, pruning and flower thinning reduce sibling competition by limiting the number of flowers. In the case of flower thinning, the production of photo assimilates remains mostly unaffected, as this technique does not remove leaves. These practices are widely recognized for increasing fruit size in many fruit crops. However, reducing competition by limiting fruitlet numbers may result in a less effective selection compared to scenarios where many siblings compete. On the other hand, cross-pollination, when other factors are not limiting, enables olive trees to reach their full production potential by increasing initial fruit set and seed size. However, larger fruits may lead to higher rates of fruit drop if the available resources for fruiting remain constant. In this context, small-fruited olive cultivars exhibit a higher proportion of flowers setting fruit, as they have reduced fruit abscission [52]. Additionally, fruit with greater genetic similarity tends to exhibit reduced sibling rivalry and, then, lower rates of fruit abortion [48]. Conversely, genetically diverse seeds intensify competition among fruit, leading to greater variability in seed and fruit size. Seed size, a critical trait, significantly influences germination, seedling survival, and growth [79,80,81]. In any case, cross-pollination benefits in self-incompatible olive cultivars are undeniable. In order to maximize fruit set, cross-pollination must occur extensively across all panicles, which requires the implementation of an effective pollination design and the careful selection of pollinizers, including their quantity and placement within the orchard. Pollinizer selection should take into account their inter-compatibility relationships and overlapping blooming periods. Other factors to consider when selecting pollinizers include the destination of the olive fruit (oil versus table), regular bearing habits, and similar vigor [27]. Contrary to this, no evidence of xenia has been reported in olive [34], although seeds (and fruit) tend to be slightly heavier under compatible cross-pollination treatments [25].

The final result is that from approximately 500,000 flowers produced in “on” olive trees, only 1–2% of them reach harvest as ripened fruit, a level still regarded as a good commercial yield [6,34]. Orchard management strategies must aim to maintain this level of fructification. This analysis is also relevant to other fruit crops that bloom in panicles, such as mango, avocado, and loquat. However, the applicability of these hypotheses must be assessed in light of the specific reproductive strategies, pollination requirements, and seeding patterns characteristic of each species.