User:Sgreene11/Pegoscapus

Mutualism

• Fig wasp ecology: Aspects of fig and fig wasp mutualism such as asynchrony among the population level of figs to provide fig wasps receptive figs throughout the year.^[1]
• Pollination ecology: morphological and behavioral specializations that are associated with host life cycle: sexual dimorphisms among fig wasps, female/male participation in life cycle^[1]
• Host utilization: host use strategies depending on if fig is monoecious or functionally dioecious^[1]
• This article highlights the fact all Pegoscapus Agaonidae do not translate all their eggs into offspring contributes to mutualism persistence and reveals the underlying mechanisms to be perhaps some eggs/larvae are unavailable or are victims of plant defenses.^[2]
• Lifetime reproductive success of lone foundresses is unaffected by the lack of oviposition in all fig ovaries. Additionally, their numbers of offspring were lower than the number of eggs carried though the wasps could lay all or almost all of their eggs. ^[2]

Reproduction and Development

• The flowering and pollination cycle of Ficus aurea and Ficus citrifolia will be described in relation to the stage of development of the fig inflorescence (synconium). The corresponding life and pollination cycle by Pegoscapus asseutus and Pegoscapus jimenezi females and males will entail entry into the fig, mating, and pollen collection. Highlighting the synchrony of fig/pollinator life cycles.^[3]
• These life and pollination cycles’ fit the general trend of Pegoscapus species’ life and pollination cycles though variability in fig inflorescence morphology correlates with variability in fig wasp morphology. Differences between species are good characteristics for phylogenetic inference.^[3]

Male Morphology

• Common characteristics of male Pegoscapus noting the seminal vesicle to have two morphologically distinct portions with the anterior portion storing mature spermatozoa and aiding reabsorption and digestive of defective cells and sperm fluid. This is reported for other wasp geneses. However, Pegoscapus has a second posterior seminal vesicle portion for ejaculation that is suggested to ensure only a small amount of stored spermatozoa are evacuated per sexual copulation. This is important as it provides each male with the ability to mate with many females rapidly and in succession in their short life spans.^[4]
• Pegoscapus differ in some features of the spermatozoa such as length, extracellular sheath thickness between species.^[4]

Female Lethal Combat

• Female agaonid wasps of a Pegoscapus showed no aggression within or outside of the fig prior to any foundress ovipositing.^[5]
• The first foundress in a Pegoscapus sp. to oviposit became aggressive leading to lethal combat and the death of the competitor. Injury, especially decapitation, was found to be effective at reducing competitors’ oviposition rates.^[5]
• However, little aggression was found in Pegoscapus tonduzi in similar contests, suggesting this reduced aggression being due to less competition for resources essential to successful reproduction due to on average fewer foundresses per flower in their native region of Panama.^[5]

Speciation

• The global and local diversity of fig and wasp species was difficult to explain based on the assumption of strict sense cospeciation and one-to-one pollinators specificity. Therefore, there is no generally accredited mechanisms on the speciation of figs and their pollinators.^[6]

• This paper suggests that hybridization and introgression due to pollinator host switches and pollinator host sharing to be the major mechanism causing diversity of fig and wasp species diversity. Hybridization leads to new genotype combinations that diversify and lead to the evolution of specialized pollinators. Additionally, the divergence is reinforced by inbreeding. Host recognition mechanisms promote pollinator divergence and speciation. Coevolution of mutualism is to be explained by semi specific wasps of a good biological species moving back and forth between figs that are not good biological species.^[6]

Cryptic Species

• Heterozygosity was found to be extremely low in the Pegoscapus species studied whereas inbreeding was found to be higher than previously estimated by non molecular methods.^[7]

• Findings suggested many fig trees may commonly be pollinated by several cryptic species.^[7]

• Micro satellite loci are vital to distinguishing cryptic Pegoscapus species for evolutionary and population genetic studies of these fig wasps.^[7]

• This paper reports coexistence of cryptic fig wasp species within a single host fig species based on genetic data with mitochondrial sequence differences implying old divergences. Some of these cryptic species’ pairs appear to be sister taxa, proving evidence for the long-term coexistence of shared hosts/colonization of novel fig species. These findings contest the strict one-to specificity between cospeciating figs and pollinators.^[8]

• This genetic information supports the relationship of observed sex ratios to predictions of local mate-competition theory as it observed higher than before levels of inbreeding and LMC. Therefore, the sex allocation theory is supported, and the precision of adaptation is highlighted.^[8]

Local Mate Competition, Inbreeding, and Sex Ratios

• This article reports confirmation of the local mate competition (LMC) theory for Pegoscapus. Local mate competition occurs when sibling males compete with one another for mating partners. This selects for female biased sex ratios and increases inbreeding levels due to mating among related fig wasps, therefore, increasing mother-offspring relatedness.^[9]

• Female bias in brood sex ratio was found. An assumption of this theory asserts each foundress wasp to contribute the same number of eggs to the brood.  This assumption causes a more female biased empirical sex ratio than expected.  If sequential oviposition occurs, the second foundress is likely to contribute less eggs to the total brood. Therefore, first-arriving foundresses lay highly female-biased sex ratios. Later foundresses then lay small, less female-biased clutches. This is done to adjust their brood sex ratio according to the LMC level or by laying males first during oviposition.^[9]

• This study determines Pegoscapus males prefer inbreeding over breeding with foreign females thus producing a female biased sex ratio. ^[10]
• Inbreeding is the mechanism that biases the sex ratio towards female because an inbred daughter carries twice the amount of a parent’s genes in comparison to an outbred daughter, increasing their reproductive value. This is true for Pegoscapus because the assumptions that the male’s only investment in offspring being sperm, and a male can mate with many females are true. For haplodiploids like Pegoscapus, more inbreeding increases predicted numbers of females. ^[10]

Conflicts With Local Mate Competition Theory

• The LMC model predicts female-biased sex ratios that increases fitness for Pegoscapus. Sex ratios have been shown to become less female-biased with increasing number of foundresses ovipositing in the same fig. This variation causes small fitness benefits compared to just biased ratios and data has shown major mismatches with the LMC theory.^[11]
• Mismatches are due to multiple foundresses typically laying too many daughters. A single foundresses' sex ratios are due to sequential oviposition and ladies-last models (wasps using their own clutch as a cue), mortality that exceeds 10% decoupling the link between primary sex ratios, focus of model predictions, and secondary sex ratios of adult wasps counted by researchers as well as frequently violated model assumptions^[11]
• Data shows wasps to lay most of their male eggs first followed by mostly female eggs deemed a “slope” strategy, resulting in more accurate sex ratios that auto-adjust to foundress number, own and relative clutch sizes and sequential clutches.  The slope strategy alters sex ratios once the capacity of a fig is crossed or when interference reduces clutch size. This suggests Pegoscapus uses a simpler mechanism to maximize fitness^[11].

Factors Influencing Reproduction

Non-pollinating fig wasps

• The sex ratio of Pegoscapus tonduzi had a positive correlation to the number of non-pollinating wasp’s independent of the number of foundresses and brood size. The number of non-pollinating wasps showed a negative correlation with the number of pollinating females. This reveals that non-pollinating wasps have a direct effect in distorting the sex ratio of Pegoscapus tonduzi broods.^[12]

• Secondary sex ratio may not precisely reveal the primary sex ratio when there is a large infestation of non-pollinating wasps.^[12]
• To understand how resources are used and adaptations are honed in Pegoscapus and fig trees, this article conducts a study on larval and gall development and finds figs entered by pollen-free wasps are more likely to abort in addition to retained unpollinated figs producing fewer fig wasps.^[13]

• Though it was thought that competition between pollinating and non-pollinating species for a viable oviposition site led to partitioning of florets between species within syconia, this study found that it does not take place. This is concluded because the offspring distribution within syconia were identical for all species including Pegoscapus silvestrii. This suggests oviposition sites not to be limiting.^[14]
• The sex ratio calculation supported predictions based on LMC and inbreeding as P. silvestrii showed stronger female biased sex ratio with less variance in sex ratio per syconium when compared to nonpollinating species. However, an increase in foundress number leads to a less female-biased sex ratio, partially contesting predictions based on LMC and inbreeding^[14]
• The sex ratio calculation supported predictions based on LMC and inbreeding as P. silvestrii showed stronger female biased sex ratio with less variance in sex ratio per syconium when compared to nonpollinating species. However, an increase in foundress number leads to a less female-biased sex ratio, partially contesting predictions based on LMC and inbreeding.^[14]

Nematodes

• Through a study on a tripartite system comprised of a fig (Ficus petiolaris), female Pegoscapus, and host-specialist nematode parasite (Parasitodiplogaster sp.), it was found that nematodes are ubiquitous in host range in Baja California Mexico, nematode infection incidence seasonal fluctuates within and between locations, and infected pollinators are sometimes correlated with fitness declines through lower levels of offspring production.^[15]
• Moderate levels of infection defined as 1-9 juvenile nematodes per host were well tolerated by Pegoscapus whereas higher levels of infection including 10 or more nematodes per host, were correlated with significant reduction in Pegoscapus lifespan and dispersal success. The overexploitation occurred in a low percentage of wasps/generation, so it was concluded that nematode infection is mostly benign.^[15]

Temperature

• This article reveals longer developmental periods for Pegoscapus with decreasing temperature.^[16]

• Wasps do not remain enclosed in their sheltered larval habitat during the winter because the decrease in temperature does not slow development enough. Winter is important as it is the season with the lowest chances of the short-lived adults to find an oviposition site.  Therefore, fig-pollinator mutualisms are constrained to the tropics because of difficult wasp persistence through the winter.^[16]

• However, the persistence of some fig-pollinator mutualisms at the northern parts of some subtropical regions still needs to be explained.^[16]  

• This study determines fig wasp life span to be significantly reduced with temperature increases predicted to occur by the end of the 21^st century.^[17]

• If Pegoscapus cannot adapt to the increasing mean daytime temperature, then their reduced lifespan will reduce the dispersion of pollination among flowering fig trees, heavily impacting the tropical forest ecosystem fig trees act as a keystone resource for by producing fruit year-round.^[17]

Second Draft:

Habitat

Pegoscapus is a genus of fig wasp in the family Agaonidae. As a pollinating fig wasp, Pegoscapus share an obligate mutualistic relationship with fig trees of the genus Ficus via association with fig inflorescences (syconia), commonly called figs.^[15] Males are smaller in size with shorter antennae than females. Males have a black head and amber-colored, wingless body. Females, however, have wings. Pegoscapus are native to the Americas, ranging from Florida to Mexico.^[18]

Mutualism

Fig wasps belonging to the genus Pegoscapus share an obligate mutualistic relationship with fig trees of the genus Ficus via association with fig inflorescences. The fig wasp and fig tree aid one another in their reproductive cycles. In their larval and reproductive stages, Pegoscapus wasps are confined to figs which provide protection and nutrients. Adult females exit the fig, collecting pollen, which they deliver to another fig inflorescence, therefore aiding in the fig reproductive cycle. This pollination mutualism has led to fig wasps developing honed morphological adaptions such as thoracic pockets to carry pollen with their forelegs to later deposit on the stigmatic surface of another fig during oviposition. Additionally, it has caused Pegoscapus to develop extreme host specificity and life cycles synchronized with the fig's reproductive cycle. For example, oviposition by fig wasps coincides with the receptivity of fig flowers, and the release of adult wasps aligns with pollen presentation. Fig phenology allows asynchronous fig development resulting in receptive figs year-round for Pegoscapus wasps.^[1]

Pegoscapus wasps lay eggs in fig trees' ovules. Each wasp larva feeds on a singular fig tree ovule. An ovule can therefore become a seed if pollinated or a "wasp gall" when the egg is deposited in it. The ovule cannot become both a seed and wasp gall. However, Pegoscapus do not oviposit in all fig ovaries even when the fig has enough female wasps with enough eggs to do so. The mutualism between figs and Pegoscapus persists in part due to the failure of all wasps to translate all of their eggs to offspring as. If they did translate all their eggs, the fig tree would not be able to produce seeds and reproduce. This occurs because some eggs and larvae are inviable or are victims of plant defenses. Moreover, lifetime reproductive success of female wasps entering the syconium is unaffected by a lack of oviposition in all fig ovaries, so this adaptation to maintain the mutualism is not harmful to Pegoscapus. Female wasps that enter a syconium are known as foundresses.^[2]

Reproduction and Development

The life and pollination cycles of Pegoscapus species varies because of the variability in fig species' inflorescence morphology that comes with being a monoecious or dioecious fig. This fig tree variability correlates with variability in fig wasp morphology in terms of pollen collection and oviposition mechanisms in order to maintain the fig wasps' and fig trees' reproductive cycles. These differences between Pegoscapus species are good characteristics for phylogenetic inferences. However, the life and pollination cycles detailed here of monoecious Ficus aurea and Ficus citrifolia and their respective pollinators, Pegoscapus asseutus and Pegoscapus jimenezi, are representative of the general trends in Pegoscapus reproductive cycles.^[3]

Monoecious syconia of these species have a globular inflorescence with pistillate and staminate florets lining a sealed cavity. The entrance into the cavity is blocked by scales during early development of the syncoium. To assess the developmental stage of the syconia and therefore its readiness for her to enter, female Pegoscapus touch the entrance with her antennae to determine the looseness of the blocking mechanisms of the fig. If loose, she passes through the tight entrance, and her wings and some antennae detach. Some fig wasps cannot fully enter and die within the entrance.^[3]

Foundresses enter the central cavity of the syconium. The eggs are oviposited into the ovary of pistillate floret resulting in wasp galls. The larvae develop there while feeding on developing seed tissues or the seed itself. After each oviposition, pollen is spread nearby via various behavioral mechanisms. Usually two or more foundresses oviposition and pollinate one syconium simultaneously. After oviposition, the foundresses die in the central cavity while the larvae and seeds continue to develop.^[3]

After 27-32 days, the central cavity swells, and males exit the ovaries where they developed. Males make up the minority of the offspring generation, lack wings, and have reduced eyes. They search for mature females that remain in the floral ovaries where they developed. The males chew holes in the ovaries and insert their abdomens to mate with the females. Multiple males begin chewing an exit tunnel in the syconium wall, and then all males die. Females widen the exit hole and emerge into the central cavity. They begin searching for anthers still containing pollen, ensuring a large enough amount of pollen is collected before exiting the tunnel. The foundresses find another receptive syconia, pollinate it, and begin the cycle once more.^[3]

Male Morphology

A common characteristic of male Pegoscapus is the seminal vesicle which produces fluids used to complete ejaculation. The seminal vesicle has two morphologically distinct anterior and posterior portions. The anterior portion stores mature spermatozoa and aides in reabsorption and digestion of defective cells and sperm fluid. The anterior portion is reported to occur in other fig wasp genera as well. Unlike other fig wasp genera, Pegoscapus has a second posterior seminal vesicle portion for ejaculation that is suggested to ensure only a small amount of stored spermatozoa are ejaculated per sexual copulation. This is important as it provides each short-lived male with the ability to mate with many females rapidly and in succession. Spermatozoa length and thickness differs between Pegoscapus species.^[4]

Female Lethal Combat

Female Pegoscapus show no aggression within or outside of the fig prior to any foundress ovipositing. However, the first foundress to oviposit in a non-specified Pegoscapus species has been found to become aggressive. This led to lethal combat and the death of the competitor by the first foundress. Injury, especially decapitation, was found to be effective at reducing competitors’ oviposition rates. In comparison to the non-specified Pegoscapus species, little aggression has been found in Pegoscapus tonduzi in similar contests. However, there were on average fewer foundresses per syconium in Pegoscapus tonduzi's native region of Panama. This suggests reduced aggression in this species is due to less competition for syconia as oviposition sites which are essential to successful reproduction.^[5]

Speciation

The global and local diversity of Ficus and Pegoscapus species has been difficult to explain based on the assumption of strict sense cospeciation and one-to-one pollinator specificity. Therefore, there is no generally accredited mechanisms on the speciation of figs and their pollinators. However, it has been suggested that hybridization and introgression due to pollinators switching and sharing hosts are the major mechanisms causing diversity of fig and wasp species.^[6]

Hybridization between Pegoscapus species results in new genotype combinations causing diversification and evolution of specialized pollinators. Inbreeding that occurs in Pegoscapus reinforces this divergence by causing these new genotype combinations to persist in the population. Coevolution of mutualism occurs because groups of genetically well defined wasp species tend to coevolve with genetically less well defined (frequently hybridizing) groups of figs. Since the fig trees have more variance in genotype, the wasp species must continually acquire adaptations to maintain the obligate mutualism in order to survive. Inbreeding reinforces these adaptations. ^[6]

Cryptic Species

Many fig trees may commonly be pollinated by several cryptic species. Microsatellite loci are vital when distinguishing cryptic Pegoscapus species for evolutionary and population genetic studies.^[7] Coexistence of cryptic fig wasp species within a single host fig species has been proven by genetic data via mitochondrial sequence differences implying old divergences. Some of the cryptic species’ pairs appear to be sister taxa, providing evidence for the long-term coexistence of shared hosts/colonization of novel fig species. These findings contest the strict one-to specificity between cospeciating figs and pollinators.^[8]

Local Mate Competition, Inbreeding, and Sex Ratios

Local mate competition (LMC) occurs when mating takes place among offspring of one or a few mothers in a discrete population. This causes brothers to compete with one another for mating partners. LMC increases inbreeding levels due to brothers competing for their own sisters as mates; this therefore increases mother-offspring relatedness. LMC favors female biased sex ratios because more females and fewer males reduces competition between males and increases mating opportunities for males. LMC occurrence is therefore supported by instances of isolated populations, high levels of inbreeding, and female biased sex ratios.^[9]

LMC has been found to occur in Pegoscapus because of the following attributes of the genus. Pegoscapus's entire reproductive cycle occurs within a fig; therefore, they have isolated populations creating competition between brothers for mates. Pegoscapus having female biases in brood (isolated sub populations) sex ratio have been found.^[9] Heterozygosity has been found to be extremely low in Pegoscapus. Inbreeding has been found to be higher than previously estimated by non-molecular methods.^[8]

Pegoscapus have a haploid diploid sex determination mechanism. This means males develop from the unfertilized eggs of their mothers; therefore, sons derive their entire genomes from their mothers. Mothers ensure their sons have high mating success and fitness by producing a female biased sex ratio in the eggs they lay. This causes the male to have ample females to mate with and low competition. This increases the mother's fitness as well because the male is then passing along the mother's genome.^[9]

Inbreeding caused by LMC is a mechanism that contributes to the formation of a female biased sex ratio because an inbred daughter carries twice the amount of the mother's genes in comparison to an outbred daughter, increasing their reproductive value. The daughter's brother has his entire genome derived from his mother, causing inbred daughters to obtain the maximum amount of the mother's genome. This maximizes the mother's fitness. This process occurs in Pegoscapus. The following assumptions to satisfy this theory are true in Pegoscapus: the male’s only investment in offspring is sperm and a male can mate with multiple females.^[10]

Conflicts With Local Mate Competition Theory

The LMC model predicts female-biased sex ratios that increase fitness for Pegoscapus. Fitness is thought to be increased by reducing male competition and increasing the number of females available for males to mate.^[9] However, sex ratios have been shown to become less female-biased with increasing number of foundresses ovipositing in the same fig. This variation causes LMC to have minimal fitness benefits as there is more competition among brothers.^[11]

An assumption of LMC theory asserts each foundress wasp contributes the same number of eggs to the brood (isolated sub population). However, if sequential oviposition occurs, the second foundress is likely to contribute less eggs to the total brood. Therefore, first-arriving foundresses lay highly female-biased sex ratios. Later foundresses then lay smaller, less female-biased clutches. This is done to adjust their brood sex ratio according to the LMC level or by laying males first during oviposition.^[9]

During sequential oviposition, fig wasps lay most of their male eggs first followed by mostly female eggs. This is deemed a “slope” strategy, resulting in more accurate sex ratios that auto-adjust to foundress number, own and relative clutch (number of eggs oviposited) sizes, and sequential clutches. The slope strategy alters sex ratios once the capacity of a fig is crossed or when interference reduces clutch size. This slope strategy is a simpler mechanism for these fig wasps to maximize their fitness during sequential oviposition rather than using LMC which has minimal fitness benefits with this occurrence.^[11]

Factors Influencing Reproduction

Non-pollinating fig wasps

Pegoscapus are a pollinating fig wasp as they collect and deliver pollen for figs. Non-pollinating fig wasps do not spread pollen. As the sex ratio of Pegoscapus tonduzi becomes more female biased, the number of non-pollinating fig wasps increased. This correlation is independent of the number of foundresses and brood size. This reveals that non-pollinating wasps have a direct effect in distorting the sex ratio of Pegoscapus tonduzi broods.^[12]

Secondary sex ratio (ratio at time of birth) may not precisely reveal the primary sex ratio (ratio at time of conception) when there is a large infestation of non-pollinating wasps.^[12] Figs entered by non-pollinating wasps are more likely to abort oviposited eggs. Retained unpollinated figs reflect higher larval mortality and lower number of fig wasps.^[13]

It has been theorized that competition between pollinating and non-pollinating fig wasp species for a viable oviposition site leads to partitioning of florets between species within syconia. However, this does not occur because the distribution of offspring within syconia have been observed to be identical for Pegoscapus silvestrii who oviposited with and without non-pollinating fig wasps that also oviposited. This suggests oviposition sites not to be limiting for neither non-pollinating fig wasps nor pollinating fig wasps.^[14]

Nematodes

Through a study on a tripartite system comprised of a fig (Ficus petiolaris), female Pegoscapus, and host-specialist nematode parasite (Parasitodiplogaster sp.), it was found that nematodes are ubiquitous in host range in Baja California, Mexico. Nematode infection incidence seasonally fluctuates within and between locations. Infected pollinators sometimes have fitness declines through lower levels of offspring production. Moderate levels of infection (defined as 1-9 juvenile nematodes per host) were well tolerated by Pegoscapus whereas higher levels of infection (defined as 10 or more nematodes per host) were correlated with significant reduction in Pegoscapus lifespan and dispersal success. The overexploitation occurred in a low percentage of wasps/generation, so it was concluded that nematode infection is mostly benign.^[15]

Temperature

Longer developmental periods of Pegoscapus correlate with decreasing temperature because winter is the season with the lowest chances of the short-lived adults to find an oviposition site due to few receptive figs. However, fig wasps do not remain enclosed in their sheltered larval habitat during the winter because the decrease in temperature does not slow development enough. Therefore, fig-pollinator mutualisms are constrained to the tropics due to the difficulty of wasp persistence through the winter. However, the persistence of some fig-pollinator mutualisms at the northern parts of some subtropical regions still needs to be explained.^[16]  

Fig wasp life span is significantly reduced with temperature increases predicted to occur by the end of the 21^st century. If Pegoscapus cannot adapt to the increasing mean daytime temperature, then their shortened lifespan will reduce the dispersion of pollination among flowering fig trees, heavily impacting the tropical forest ecosystem. Fig trees act as a keystone resource by producing fruit year-round.^[17]

Figs and fig wasps in general are most abundant in the equatorial tropics. The flowering frequency of figs declines in colder and drier areas. This decreases the availability of receptive syconia for Pegoscapus to oviposit in, leading to local extinction of fig wasps and subsequent reproductive failure of figs. This limits the fig wasp mutualism to the tropics. However, the persistence of some fig-pollinator mutualisms at the northern parts of some subtropical regions still needs to be explained.^[16]