Incestuous fig wasps: death in paradise [HD]

0:09 fig trees have played a role in human diet and culture for thousands of years they produce great bounties of fruit seemingly without flowering by hiding their flowers within the inflorescences that ripen into the figs we eat across the tropics and subtropics there are over 750 species of fig tree their fruits are responsible for feeding over a thousand species of birds and mammals and yet they can only do so thanks to a remarkable relationship with an insect scarcely a millimeter in length the fig wasp

0:57 the Queen Sirikit Botanic Garden in northern Thailand is home to several types of fig tree including Ficus racemosa and Ficus hispida which fruit year round and have species-specific obligate mutualisms with fig wasps Ficus racemosa is a large tree reaching between 25 and 40 meters tall it is usually found growing near rivers and bears two to seven fig crops a year these figs grow along the trunk and boughs in dense clusters each mature fig growing up to five centimeters across and turning orange red when ripe Ficus hispida is a smaller bushier tree reaching between 3 and 10 meters in height

1:47 it is a pioneer species good at colonizing open spaces riversides and roadsides with numerous small hairy figs growing from long runners hanging from its trunk when mature the figs turn yellow and grow to around 3.5 centimeters in width Ficus hispida is a functionally dioecious tree which produces an average of five crops per year with slightly more crops occurring on female trees than males these crops are asynchronous and so an individual tree can have figs at multiple developmental stages at any one time Ficus racemosa is monoecious and fruits synchronously within a tree but asynchronously between trees

2:40 this helps to limit inbreeding and ensure that a population of the short-lived pollinator wasp survives at any one time Ficus racemosa is pollinated by the wasp Ceratosolen fusciceps only when the female flowers within the fig are receptive to pollination does the fig try to attract its pollinator it does so by releasing species-specific volatile compounds to grab the attention of nearby wasps compounds which are different in composition to those produced at any other fig stage and from those of any other species

3:32 this can result in some competition to access the flowers but usually only a few will be let in however despite being invited the process of entry is not easy a female fig wasp must enter the fig through a small opening called the ostiole she uses her wedge-shaped head to force herself between the bracts that guard the opening her antenna scapes flattening into grooves on her head the gap is tight and so she allows the rest of the moisture she carried for her journey to be squeezed out she no longer has a need for it as it is likely that she won't be leaving this fig again

4:22 Ficus hispida is pollinated by the wasp Ceratosolen solmsi these females have a shorter ovipositor helping to distinguish them from those of Ceratosolen fusciceps they too must enter the figs quickly to avoid the jaws of hunting ants a female wasp that enters through the ostiole successfully does so at the cost of her wings and most of her antennal flagella which are torn off her body to allow passage into the fig

5:11 she uses tooth-like structures on her fore and hind tibia and extended mandibles with rear pointing ridges to pull herself between the bracts to stop her slipping backwards soon she finds herself within the hollow fig cavity it is lined with a carpet of translucent female flowers and it is down the styles of these flowers that she will begin to lay her eggs a behavior so ingrained that female wasps even seem able to do so without a head

6:00 she carefully lays a single egg besides the ovule of each flower and injects a secretion to induce the ovary to grow rapidly and form a gall in which the wasp larva will grow in exchange for this safe nursery the fig tree requires its own reproductive needs to be met most flowering plants are pollinated passively the pollinators visit the flowers for food and gather pollen inadvertently transferring it from plant to plant without any specific behavior however both Ficus racemosa and Ficus hispida are pollinated actively by their pollinator wasps

6:51 the wasps possess specialized pollen pockets on the underside of their thorax from which they carefully unpack pollen grains and dab them onto the stigmas into which they will lay an egg Ficus racemosa is a monoecious fig tree therefore every individual tree produces figs which supply both pollen and seeds the flowers within these figs are densely packed with their ovaries at a range of depths from the fig wall the pedicels and styles of these flowers vary in length allowing the stigmas of all the individual flowers to be level and form a single large synstigma

7:41 the Ceratosolen fusciceps females probe the styles and generally only lay eggs in shorter styled flowers leaving the lower ovaries to develop into seeds by closing the ostiole the fig tree can potentially limit the number of female wasps entering each fig and in doing so ensure that the number of accessible ovaries inside exceeds the number of eggs carried in by the wasps this ensures production of fig seeds

8:27 functionally dioecious fig trees like Ficus hispida have a different strategy as they keep production of seeds and wasps on separate trees however the female pollinator wasps cannot distinguish between them as they smell the same female wasps arriving into the male figs of Ficus hispida find a carpet of identical short-styled female flowers all of them accessible for oviposition and growth of young wasps however a female wasp that is unlucky enough to enter the fig of a female tree will find a different arrangement the flowers within these figs all have stigmas unsuitable for inserting ovipositors and yet the female wasps will pollinate them and attempt to oviposit in vain

9:19 ultimately only leading to production of fig seeds after pollination and oviposition the female fig wasps usually die within the fig cavity and the figs begin to ripen inside the larval wasps develop and grow within their individual gall flowers they consume the entire contents of the fig ovary until only the outer shell of the gall remains

10:05 after a period of as little as 30 days the first adult wasps begin to stir using their strong mandibles to chew an exit from their galls it is the males who emerge first fig wasps show extreme sexual dimorphism the crawling golden males looking very different to their female counterparts these males of Ceratosolen fusciceps are adapted for life in the dark encircling landscape of a fig possessing poor eyesight short limbs and a soft telescopic abdomen

10:53 the males of Ceratosolen solmsi are similar but appear to lack functional eyes and their heads are paler and more rectangular than those of Ceratosolen fusciceps once in the fig's cavity the males begin to chew into the galls of the neighboring female wasps they channel their telescopic abdominal segments guided by their head into the galls in order to mate with the females many of whom will be their sisters fig wasps have a haplodiploid sex determination system the haploid males are mainly laid first from unfertilized eggs and the diploid females formed from fertilized eggs are mostly laid second

11:49 the sex ratio of a brood hatching within a fig is highly female biased with up to six times more females than males when multiple female wasps are laying eggs within a single fig the sex ratio of a brood changes this is because as competition for oviposition sites increases most of the remaining eggs that go unlaid will be the females these scarce males are precious and so are usually located in the innermost galls more protected from parasitoid wasps attempting to oviposit through the fig wall this results from the males being laid first giving their gall flowers a head start to expand into the center of the fig

12:42 as the figs of Ficus racemosa mature they fill with fluid and the remnants of this can remain even as the males start to emerge although the pollinator wasps generally keep to the tops of the galls as they look for females the slender males of non-pollinating Apocrypta fig wasps navigate the watery areas in between the females they seek mostly occupy galls closer to the fig wall and so these males possess tubes on the tips of their abdomens which act like snorkels as they search their spiracles are surrounded by water repellent hairs to further ensure that they can breathe

13:27 by widening the holes left by the males who impregnated them the female wasps begin to emerge from their galls often shedding the last pieces of pupal exuviae off their antennae as they push out into the fig

14:19 as the wasps developed so too did the figs male flowers the anthers matured and split open revealing vertical slits filled with pollen using their front tarsi the fig wasps slowly and diligently gather pollen from the anthers and stuff it into their special thoracic pollen pockets by scraping from one side to the other the pockets are fringed with a comb of hairs which aid pollen collection and removal and Ceratosolen solmsi females seem able to collect pollen at a median rate of close to one stroke per second

15:13 for actively pollinated figs such as Ficus racemosa and Ficus hispida such pockets ensure that some pollen travels to the figs in which the wasps will lay their eggs despite the tight squeeze through the ostiole and a journey of up to 150 kilometers for some fig wasp species this efficient method of pollination means that unlike in passively pollinated fig trees actively pollinated fig trees need not invest in having large numbers of male flowers other organisms are preparing to leave the fig too juvenile nematode worms likely of several different species reach out into the fig cavity waving until they touch a female fig wasp

16:02 upon contact they quickly enter her body or take refuge in the folds of her abdomen with the hope of traveling with her to another fig those female wasps carrying just a few nematodes will likely be unhindered by their presence but those who accumulate too many may find their lives shortened and their ability to disperse reduced meanwhile the males set about their next task to create a tunnel through which the females can leave their natal fig they work together chewing a path to the outside world usually through or close to the ostiole

17:09 several hours later they emerge into the open air and begin piling up clumsily on the fig their anatomy unsuited to walking on such a surface this event attracts unwelcome predators ants are drawn by the odor of the emerging wasps and mature fig and are seeking an easy meal by emerging first the male wasps are far more likely to get eaten when just a few ants are present the initial outburst of male wasps distracts and occupies the ants long enough to allow most of the females to take flight and seek a receptive fig of their own

18:09 however too many ants and the tiny wasps are outnumbered the pollinator wasps are also accompanied by a procession of Chalcid non-pollinator fig wasp females their ovipositors vastly longer than their bodies their mothers laid them as eggs through the fig wall using an array of sensilla concentrated along the length and tip of their ovipositors to guide them to the fig flowers within these parasitoid and gall forming wasps are longer lived than the pollinators and will set off to find receptive figs in which to deposit their own offspring

19:24 the females of Ceratosolen fusciceps with just a day left of life will fly high above the canopy here the wind will carry them part of the way to a receptive tree like the pollinators of other sparsely populated monoecious fig trees those of Ceratosolen solmsi will likely find a receptive male fig tree closer to home with figs in which to start their life cycle once more