What’s (not just) brown and sticky? Adaptive radiation in Stick and Leaf Insects in the order Phasmatodea.

-1
The Indian or laboratory stick insect, Carausius morosus, a common pet.

The order Phasmatodea contains more than 3,000 extant species of insect found throughout the world, especially the warmer zones. These herbivorous (mostly arboreal) insects are most well-known for their crypsis, or camouflage, where their colour, shape and behaviour enable them to masquerade as twigs or leaves (hence their common names of stick and leaf insects).

Though there is still uncertainty about a definitive phylogeny, phasmids are considered one of 11 orthopteroid insect orders within the assemblage known as Polyneoptera. Phasmatodea are found alongside the modern orders: Blattodea (cockroaches), Dermaptera (earwigs), Embioptera (web-spinners), Grylloblattodea (ice crawlers), Mantodea (praying mantises), Mantophasmatodea (heel-walkers) and, of course, Orthoptera (crickets, grasshoppers, and katydids). According to phylogenomic analyses of nucleotide and amino acid sequences, some of these Polyneopteran lineages are thought to have emerged ~302 million years ago, with phasmids evolving after the Permian mass extinction.1

Fossil Evidence

Fossil evidence of phasmids is, however, extremely rare.   Specimens have been recovered in amber, most notably representatives of Euphasmatodea and Timematodea, with the oldest well-documented fossils being found in Cretaceous Burmese amber. Recent discoveries of the oldest-known fossilised leaf mimics (Phylliinae) from Messel, Germany in 2006 of Eophyllium messelensis date this foliacious mimicry to the Eocene.2

Although the fossil evidence is patchy, it is thought that traits relating to morphological plant masquerade within Phasmatodea first developed with stick mimicry in the Permian, followed by leaf mimesis developing in the Eocene when angiosperms largely replaced conifers as dominant trees.

phasmid fossils
Simplified cladogram with a partial geochronologic scale showing the phylogenetic position of E. messelensis and the temporal sequence of character evolution. Insert; Photo (A) of holotype of fossil leaf insect E. messelensis, from the Eocene Messel Pit, Germany and Photo (B) Cretophasmomina melanogramma from 126 mya from the Yixian formation in Inner Mongolia [2, 3]
Fossils of Cretophasmomima melannogramma discovered in Yixian, China in 2006 from the Cretaceous Jehol biota (approximately 129 mya), however, provides evidence of phasmid crypsis relating to a Gingkophyte, Membranifolia admirabilis, which displayed leaf-shaped plant organs.3  It is therefore thought that leaf mimesis may well have developed far earlier than previously thought.

Crypsis, Camouflage, and Masquerade

In order to avoid visual detection by predatory mammals, birds, reptiles and other invertebrates, many insects evolved morphological characteristics that enabled them to blend in to their surrounding environment. Specifically in the case of phasmids, these evolutionary adaptations have been very closely linked to the insects’ host and food plants leading to a coupling of ecological and evolutionary dynamics.4,5,6

Cryptic colouration, elongation of the body and legs, or, alternatively, broadening and flattening of the body to resemble leaves are all forms of masquerade adopted by phasmids to avoid detection by predators. This has led some researchers to conclude that predation may be an important driver of speciation in this order. Successful adaptation, through camouflage, may therefore lead to divergence in adaptive radiation. 4,5,6  

The basal-most extant recorded clade of Phasmatodea is the sub-order Timematodea, within which is found the genus Timema whose species are found throughout southwestern North America on a variety of host-plant species.7 Experimental studies have been conducted into the influence of ecological factors with regards adaptive radiation in Timema cristinae with particular emphasis on host plants and cryptic colouration.4,5,6,7

 

cladogram
Above: Timema cristinae, endemic to California has repeatedly evolved ecotypes adapted to different host plant species. One ecotype features a distinct white stripe (right photo) on its back and feeds on the thin, needle-like leaves of a shrub called Adenastoma. The other phenotype has no stripe and feeds on Ceanothus (left). Below: Phylogeny of Timema species.

It was found that two distinct T. cristinae morphs had developed on two morphologically dissimilar plant species distributed in parapatric mosaics. The first plant, Adenostoma fasciculatum, has needle-like leaves, while the other, Caenothos spinosus, has broad, ovate leaves. Each T. cristinae morph (or ecotype) was found to be more cryptic on one of the two plant species depending on whether they displayed a heritable white dorsal stripe or not. One of the experiments found that bird predation significantly lowered numbers of T. cristinae that were maladapted to the host plant. Further studies concluded that through predator pressure, partial (but incomplete) ecological speciation has occurred in T. cristinae as the morphs still successfully interbred.5,6,7

This partial speciation may, however, form only one dimension of selective pressures that constitute adaptive radiation events. It was also shown that by comparing different Timema species that share the same host plant, that sexual isolation was not as marked as with between species on different plants (when compared with T. podura and T. chumash)7 lending credence to the notion of ecological speciation. It is therefore apparent that predators apply selective pressure leading to morphological crypsis and divergence, but that this does not necessarily directly lead to speciation, but is more likely an intermediate stage in adaptive radiation.

Flying, Jumping, and Holding Still

In the case of the Phasmatodea, it has been discovered that diversification occurred in a wingless state and that wings were subsequently derived on a number of occasions.

Of the 3,000 species of phasmids, only 40% are fully winged, while the remainder are partially winged or entirely wingless. While being fully winged conveys advantages of dispersal, escape and finding resources,  it has been claimed that increased female fecundity and crypsis may have served as a selective advantage in early phasmid evolution in a shift to winglessness. Apart from flight, wings and partial wings can also be used in threat or startle responses to deter would-be predators. By examining DNA sequence data and applying parsimony optimisation it was found that the ancestral condition of Phasmatodea is wingless.8

It was also found that certain phasmid lineages had “re-evolved” wings prompting suggestions that this reacquisition may confer adaptive advantages of being both winged and wingless as conditions necessitate over ecological time leading to further speciation.8

phylogeny

Timema chumash is unusual in phasmids in that it has been found to jump away from potential threats. Although it can only jump relatively short distances by extending the hind tibia, it can reach take-off velocities comparable to some larger European flea beetles. The leg positions and hind-leg length of T. chumash contrast with the morphology of other stick insects; its legs emerge ventrally from the thorax and its hind legs are proportionately longer than those of other phasmids. As T. chumash is wingless, it jumping is suggestive that it would enable a rapid fall from the plant it was perching on taking it out of the visual field of predators and providing it with another opportunity to camouflage itself nearby.9 These morphological and behavioural traits may present opportunities for further adaptive evolution.

crypsis

A well-documented behaviour in many phasmids is that of catalepsy whereby the insect is able to remain motionless or produce extremely slow movement as a form of twig or leaf mimesis to aid with predator evasion. The mechanism by which this is achieved, is via the high gain of the femur-tibia joint control system,10 and has been recorded in fossil specimens.2  A key difference between phasmids and other orthopteroids is this significant coevolution of the mimetic body shape with catalepsy.10

Parthenogenesis, Hybridogenesis and Androgenesis 

Phasmids experience a wide array of reproductive modes with about 10% of the phasmid taxa being parthenogenetic and producing all-female offspring (thelytoky).11 Although parthenogenesis reduces genetic variability, it does not wholly suppress it.  Furthermore autopolyploids and allopolyploids can take advantage of higher mutational rates to increase heterozygosity. Androgenesis is also common and has been proposed as a likely pathway to cladogenesis in the genus Clonopsis11 and has already been recorded in Pijnackeria where tetraploid hybrids lacking maternal genes, but keeping the maternal mitochondrial DNA, speciated.12 The discovery of interracial and interspecific hybridogenesis in the genus Bacillus added further weight to the notion of maintaining (or even increasing) genetic diversity within phasmid lineages and creating opportunities for further speciation. 12  

No one reproductive mechanism is exclusively used, so that complete reversion from thelytoky to amphimixis is possible.  These “tangled interactions” allow for genetic diversity to persist within and between populations. When considered as part of a series of repeated and complex reproductive strategies including sexual reproduction, parthenogenesis, androgenesis and hybridogenesis, it must be concluded that evolutionary pathways for phasmids are far from dead-ends.11, 12

Following divergence from other orthopteroids, phasmids took advantage of the new food sources and flourished following the angiosperm revolution and have continued to adapt in relation to predatory pressures, host-plant availability, behaviours, and complex reproductive strategies. Clearly, apart from the opportunities presented in the Eocene for cladogenesis and speciation, there continues to be further evolutionary opportunities relating specifically to morphology and sexual isolation in adaptive radiation of phasmids.

Black beauty stick insect shutterstock_51123130-1
The Black Beauty stick insect, Peruphasma schultei, is known to exist only in a tiny area of 5ha (12 acres) in the Cordillera del Condor region of northern Peru, at altitudes between 1200-1800m.

References:

1.  Misof, B.  et al. (2014), Phylogenomics resolves the timing and pattern of insect evolution. Science. 346 (610), 763-767.

2. Wedmann, S., Bradler, S., and Rust, J. (2006), The first fossil leaf insect: 47 million years of specialized cryptic morphology and behavior. Proceedings of the National Academy of Sciences. 104 (2), 565-569.

3. Wang, M., Be´thou, O., Bradler, S., Jacques, FMB., Cui, Y., and Ren, D. (2014), Under Cover at Pre-Angiosperm Times: A Cloaked Phasmatodean Insect from the Early Cretaceous Jehol Biota. PLoS One, 9 (3), e91290

4. Farkas, TE., Mononen, T., Comeault, AA., Hanski, I. and Nosil, P. (2013) Evolution of Camouflage Drives Rapid Ecological Change in an Insect Community. Current Biology. 23, 1835-1843.

5. Nosil, P., Crespi, BJ., and Sandoval, CP. (2002) Host-plant adaptation drives the parallel evolution of reproductive isolation. Nature. 417, 440-443.

6. Nosil, P. and Crespi, BJ. (2006) Experimental evidence that predation promotes divergence in adaptive radiation. Proceedings of the National Academy of Sciences. 103 (24), 9090-9095.

7. Nosil, P. and Sandoval, CP. (2008) Ecological Niche Dimensionality and the Evolutionary Diversification of Stick Insects. PLoS One. 3(4), e1907

8. Whiting, MF., Bradler, S. and Maxwell, T. (2003) Loss and recovery of wings in stick insects. Nature. 421, 264-267.

9. Burrows, M. (2008) Jumping in a wingless stick insect, Timema chumash (Phasmatodea, Timematodea, Timematidae). The Journal of Experimental Biology. 211, 1021-1028.

10. Wolf, H., Bässler, U., Spieß, R. and Kittman, R.  (2001) The femur–tibia control system in a proscopiid (Caelifera, Orthoptera): a test for assumptions on the functional basis and evolution of twig mimesis in stick insects. The Journal of Experimental Biology. 204, 3815-3822.

11. Scali, V. (2009) Stick insects: parthenogenesis, polyploidy and beyond. In: Life and Time: The Evolution of Life and its History. Cleup, Padova. 171-192

Mosquito extinction. Is it really a good thing?

Anopheles_stephensi.jpeg

A few years ago I read an op-ed piece in the journal Nature that celebrated the potential demise of mosquitoes as scientists prepared to release genetically modified mosquitoes in Brazil in an attempt to eradicate populations carrying malaria. What most struck me about the piece was that the author concluded that mosquitoes performed no ecological function and that the world would be a better place without these pestiferous nuisances. This statement left me feeling a little uneasy. How certain could we actually be that mosquitoes performed absolutely no ecological function?

“Eradicating any organism would have serious consequences for ecosystems — wouldn’t it? Not when it comes to mosquitoes…”

In 2014 I listened to a podcast produced by Radiolab that reiterated the pointlessness of mosquitoes and again I wondered whether this could really hold entirely true. Apart from David Quammen’s valiant effort to convince us of the mosquito’s general innocence (it is after all only the females that bite, and even this is only in order to produce young). He also asks us to imagine just how quickly deforestation and exploitation of the tropics would have progressed without the relative protection afforded by the mosquito and all of it’s diseases.

 

According to the World Health Organisation (WHO) 17% of the global estimate of all infectious diseases are vector-borne. Of these, mosquito-borne diseases constitute the majority, with malaria causing an estimated 627,000 deaths in 2012 and infecting 1.5 to 2.7 million people a year. Some of the other mosquito-borne diseases that affect humans are Dengue fever, West Nile virus, Yellow fever, Lymphatic filariasis, Japanese encephalitis, Rift Valley fever, and Chikungunya; causing death, suffering and both social and economic hardship.
There are approximately 3,500 named mosquito species in the world. They are found in a variety of habitats in every biogeographic region apart from the Antarctic. Of these, only 40 Anopheles species are known to be effective transmitters of human malarial infection and only around 350 species are regarded as effective in all mosquito-borne human disease transmission.  The catholic nature of mosquitoes in relation to habitat selectivity is best illustrated in the breadth of the geographic area covered by dominant malarial Anopheles mosquitoes.  Mosquitoes are highly speciose, with the greatest species diversity being found in the Neotropical regions as shown in the map below.

 

tileshop.fcgi

This preponderance of mosquitoes to cause such human hardship has led to a variety of campaigns designed to control and eradicate them; from the use of DDT in the 1940s to attempts to sterilise males through exposure to radiation. Though there has been some success with these methods in the past, elimination of mosquitoes in the tropics has always proven difficult due to mosquito resistance, pathogen resistance to treatments, the lack of infrastructure and financial support. Conventional means of avoiding infection from mosquito-borne diseases have been to prevent being bitten through the use of mosquito nets and chemical repellents. I was therefore rather intrigued to hear about the work of Oxitec, the Alphey Lab and others in relation to developing genetic controls to exterminate this “winged scourge”.

The ecological niche filled by mosquitoes is little understood and has been poorly studied. In 2010, at the British Ecological Society’s annual meeting, the chair, Professor Charles Godfray said:
“We know very little about the [mosquito] community ecology… and this is significant because if you were to knock it out then you want to know what would take its place. […] And we don’t know enough, not for the want of trying, about the dispersal of the mosquitoes; how they move from one place to another.”
I simply couldn’t believe that such a large knowledge-gap existed with regards such an ubiquitous insect, so I decided to survey the scientific literature to figure out what is currently understood to be the ecological function performed by mosquitoes. I found that a very small number of papers actually concerned themselves with this topic directly and those that did were generally in relation to highly specific niches like larval processing of detritus chain interactions within pitcher-plants, the pollination of orchids, or focused on other species entirely, such as reindeer and caribou whose migration behaviour is influenced by the predation of mosquitoes and other biting flies. Understandably, most papers concentrated on the mosquito as disease vector – especially in relation to humans – but, apart from noting that mosquitoes constitute an enormous biomass, are found in both freshwater and terrestrial ecosystems at different life stages, and that they are highly speciose; there has been little scientific research into their ecological significance. We can extrapolate that they must be an important food source for a number of other insects, birds, reptiles, fish, amphibians and even mammals, but the data is lacking to support this – we need more research to be conducted to be certain. There is also a possibility that mosquitoes contribute to a disease dilution effect, but further study would be required to support any such claim.
So, is it a good idea to locally exterminate mosquitoes if we really don’t have any idea what will happen to their ecosystems? I would suggest that it probably isn’t the greatest idea. Possible scenarios are a reduction in available food for predators that will cause greater predation on other food sources thereby decreasing these at a faster rate and increasing competition. Increased competition can in turn lead to lower reproductive success and in the worst-case scenarios population collapse of apex predators. At least, I think it would be safe to assume that those ecosystems would no longer operate in the same way – their species composition would shift  to a greater or lesser degree and with that the functional ecology.

And what about the disease dilution effect? Well, if it holds true in the case of mosquitoes then we may witness an intensification of disease virulence and higher infection rates. An alternative hypothesis is that the pathogens might move into other host species and we would be left scrabbling for new control mechanisms.

As someone with a desire to understand the intricately interlinked nature of our world and all the living creatures in it, I couldn’t support the deliberate extinction of any species (despite the detrimental effects it can have on humanity) without first knowing what the knock-on effects of that extinction would be. In doing something that we hope would benefit humanity, we may in fact be creating new and more complex problems.

An American entomologist, Jeremy Lockwood, wrote of the need to establish an ethical basis of “philosophically sound, scientifically consistent” considerations with regards our relationship to insects. He proposed that we refrain from taking actions that would kill or cause nontrivial pain to insects, but not if by avoiding those actions there would be nontrivial costs to human welfare. Genetically modified mosquitoes, and by association other mosquito control mechanisms, would presumably be considered acceptable to most people within this  anthropocentric ethical framework. The irony of this position however is, as Lockwood points out, that a person considered a humanitarian is often referred to as, “one who wouldn’t hurt a fly”.
This blogpost is based on my final-year research paper. For those of you wanting a bit more in-depth information, you can read the full paper here.

References:

Alphey, L. (2014). Genetic Control of Mosquitoes. Annual Review of Entomology59(1), 205–224. doi:10.1146/annurev-ento-011613-162002

Fang, J. (2010) Ecology: A world without mosquitoesNature News, 466(7305), 432–434. doi:10.1038/466432a

Godfray, H. C. J. (2013). Mosquito ecology and control of malaria. Journal of Animal Ecology, 82(1), 15–25. doi:10.1111/1365-2656.12003

Lockwood, J. A. (1987). The Moral Standing of Insects and the Ethics of Extinction. Florida Entomologist70(1), 70 – 89.

Sinka et al. (2012). A global map of dominant malaria vectorsParasites & Vectors5(69). doi:10.1186/1756-3305-5-69

World Health Organisation http://www.who.int/whr/1996/media_centre/executive_summary1/en/index9.html.

 

Hawk moths and evolutionary predictions

tumblr_nyja9lfDoo1qbsotxo1_1280
A selection of Sphingidae moths photographed from the collection at London’s Natural History Museum.
Commonly known as Hawk Moths, Sphinx Moths and Hornworms, these moths are important pollinators of orchids and other flowers.
Nectar tubes and hawk moth tongue lengths are often associated; Xanthopan morganii praedicta (centre) was famously predicted to exist by Charles Darwin and Alfred Russel Wallace based on the length of the nectar spur of the Madagascan Christmas star orchid (Angraecum sesquipedale). Note the length of the moth’s uncoiled proboscis in the photo above.
In a letter to Joseph Hooker in 1862, Darwin wrote:

“I have just received such a Box full […] with the astounding Angraecum sesquipedalia [sic] with a nectary a foot long. Good Heavens what insect can suck it.” 

KPPCONT_047171
A hand-coloured lithograph of Angraceum sesquipedale by W.H. Fitch (1859) taken from Curtis’s Botanical Magazine.

A few days later, Darwin wrote a second letter in which he postulated that this insect must be a moth, and in 1867 Wallace published an article in which he supported Darwin’s suggestion, remarking that the African hawkmoth Xanthopan morganii (then known as Macrosila morganii) had a proboscis almost long enough to reach the bottom of the spur. In a footnote to this article Wallace wrote:

“That such a moth exists in Madagascar may be safely predicted; and naturalists who visit that island should search for it with as much confidence as astronomers searched for the planet Neptune,–and they will be equally successful!”

In 1903 (41 years after Darwin’s observation) this moth was discovered and named by Rothschild & Jordan after Wallace’s prediction that the moth would in fact be a hawkmoth. However, it was not before 1997 that it was finally confirmed that the Madagascan Christmas star orchid is actually pollinated by Xanthopan morganii praedicta. 


 

Further reading:
Darwin and Wallace’s Predictions Come True

Angraecum sesquipedale

Miller, W. E. (1997) ‘Diversity and evolution of tongue lengths in Hawkmoths (Sphingidae)’. Journal of the Lepidopterists’ Society. 51(1), 9-31

Wasserthal, L. T. (1997) ‘The pollinators of the Malagasy star orchids Angraecum sesquipedaleA. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift’. Bot. Acta 110: 343-359