evolution – Ecology Field Notes

Faking it as a survival strategy

Cheats and Deceits: How animals and plants exploit and mislead. By Martin Stevens. Published by Oxford University Press (2016).

Last year, on a trip to Devon, I saw my first ever oil beetle (Meloe proscarabaeus). She was beautiful. Her black carapace glistened violet and blue in the sunlight. She was gravid and crawling along the footpath in search of a place to dig a nest burrow to lay her eggs. But what I did not yet appreciate was the extraordinary life cycle of these captivating beetles. The young of a related species, Meloe franciscanus, emerge from the nest and swarm up a nearby plant where they congregate in a mass mimicking the shape of a female solitary bee (Habropoda pallida) and release a chemical compound similar to the bee’s sexual pheromones. This proves all too irresistible to male bees who are drawn to this aggregation and attempt to mate with it, presenting the larvae with the perfect opportunity to grab hold of the bee and clamber onto his back. He then carries these passengers with him until he finds a female to mate with at which point the larvae instantly decamp onto the female. From here they then transfer to her nest where they devour the stored nectar, pollen and the bee’s eggs. The evolution of this complex mimicry is absolutely fascinating and forms part of Martin Stevens‘ interrogation of deception in Cheats and Deceits: How animals and plants exploit and mislead.

This book is an immensely informative and enjoyable exploration of the multiple roles deception plays in nature. Stevens sets out a detailed examination of a wide variety of instances of natural deception from well documented examples such as the evolution of camouflage through industrial melanism in the Peppered Moth (Biston betularia) to current research into the resemblance to falling leaves in the movement and colouration of Draco cornutus, a gliding lizard from Borneo. It is to Stevens’ credit that this book makes for entertaining and effortless reading while clearly citing all the relevant research within context and pointing to areas where knowledge is still lacking.

The language of deception is important. Stevens takes the time to explain some of the more commonly used terms associated with deception such as camouflage (blending in to the environment), mimicry (assuming the appearance – be that visual, chemical, behavioural or acoustic – of another organism) and masquerade (taking the form of an inedible object – as with stick insects). Mimicry and masquerade therefore lead to misidentification while camouflage reduces detectability or impairs recognition. Mimicry also comes in various guises some of which can be described as: aggressive, when predators mimic harmless species to enable prey capture; Batesian, when a palatable species mimics the characters of an unpalatable species, as seen in the chicks of an Amazonian bird Laniocera hypopyrra mimicking toxic caterpillars; and imperfect mimicry, as with hoverflies roughly resembling certain species of wasps and bees (for which there are a number of competing theories).

This, of course, only scratches the surface of a vast area of research that Stevens specialises in as head of the Sensory Ecology and Evolution group at the University of Exeter where he continues to research these themes. His enthusiasm for his topic is highly infectious; you find yourself transported from an explanation of background matching in cuttlefish, to an historical aside concerning the development of military camouflage, and on again to a description of his own field experiments in testing the efficacy of disruptive colouration.

“We must trust to nothing but facts: these are presented to us by nature and cannot deceive. We ought, in every instance, to submit our reasoning to the test of experiment, and never to search for truth but by the natural road of experiment and observation.” ~ 18th-century chemist Antoine Lavoisier

The book does rely heavily on zoological examples, and although Stevens doesn’t entirely neglect plants his observations do tend to mainly focus on carnivorous plants and orchids. But to be fair, Stevens does make the point that more research into botanical forms of deception is required and suggests that this should be undertaken with a view to specifically exploring the roles of chemical signalling and sensory exploitation. One of the examples cited in the book is the orchid Epipactis veratrifolia which attracts female hoverflies to lay eggs on the plant by releasing chemicals that mimic the alarm pheromones of aphids (the food source of hoverfly larvae). This may rather be a means by which the orchid exploits an inbuilt perceptual preference for chemicals associated with hoverfly larval food sources – either way the plant is deceiving the insect in order to ensure protection from aphid infestation.

A form of deception more commonly associated with orchids is that of exploiting male insects to pollinate plants by mimicking the female form through the shape and colouration of the flower. However, Stevens points out that this mimicry is sometimes (as in Cryptostylis orchids) not particularly convincing to human eyes, but is overwhelmingly so to the male wasp which tries to mate with the flower and thus collects the pollinium which will be deposited at the next Cryptostylis flower that he visits. With this example (as with the oil beetle, among others) the author cautions researchers of deception in nature to be aware of anthropocentric biases that may arise through our observations and study, and to (wherever possible) approach our subjects in the manner and with the senses of the deceived species.

I am utterly delighted and inspired by this book and am certain that I will return to it again and again as a point of reference. I have no hesitations in highly recommending it to researchers, field naturalists and those with a passing interest in natural history.

Postscript

At the time of writing, Phil Torres and Aaron Pomerantz have discovered and documented kleptoparasitism of ants in a species of butterfly (Adelotypa annulifera) in the Peruvian Amazon which they believe might mimic ants through their wing patterns. This seems to me an ideal opportunity for further research looking at visual and chemical mimicry given both the wing patterns and larval associations.

The Little Bombardier

Best stay out of the way.

There are more than 500 species of Bombardier beetle (a form of ground beetle – Carbidae) in the tribes Brachinini, Paussini, Ozaenini, or Metriini all displaying the highly effective defence mechanism of releasing a superheated pulsing jet of noxious chemicals sprayed directly at would-be predators. I have always been fascinated by the ammunition of Bombardier beetles – their highly accurate and violent chemical attack brought on whenever you touch them – but it was only on reading Eisner’s essay that I started to fully grasp the incredible complexity of these beetles.

These diagrams are reproduced from Thomas Eisner’s fascinating book For Love of Insects which explores the variety of ways in which insects use chemicals for defence, signalling and prey capture. I cannot recommend this book highly enough for anyone interested in the pursuit of entomology or study of chemical ecology.

Screen Shot 2015-12-04 at 07.33.26 — Diagram of a bombardier beetle with its 2 glands in place. R = reservoir; r.ch = reaction chamber; gl = glandular tissue; dt = duct

Screen Shot 2015-12-04 at 07.38.01 — The mechanism of operation of the bombardier glands. E = enzymes in the reaction chamber; R indicates that either a hydrogen (H) atom or a methyl group (CH3) can occur at that site on the hydroquinone or quinone molecule.

The chemical process involves hydrogen peroxide rapidly decomposing into oxygen and boiling water, while the hydroquinones oxidize into benzoquinone in the beetle’s reaction chambers. This mix explodes out of the beetle with an audible popping sound, in a volley of rapid-fire blasts – in a manner likened to the pulsing propulsion system of Germany’s V-1 “buzz bomb” in WWII. The consequent foul chemical burn (at 100°C) incapacitates smaller attackers like ants, and deters larger predators such as the unfortunate frogs in one of Eisner’s experiments.

By examining the propulsion mechanism using high-speed synchrotron X-ray imaging Eric Arndt from MIT confirmed Eisman and his colleagues’ qualitative passive ‘pulse jet’ model. This research shows that a flexible membrane and a valve passively control the spray pulsation – as pressure increases in the reaction chamber because of the chemical explosion, the membrane stretches and the valve closes. The membrane then relaxes and the valve reopens once the pressure has been reduced following the ejection of the liquid, and so the process repeats.

The only UK resident species of bombardiers are Brachinus sclopeta, the streaked bombardier beetle, and Brachinus crepitans, the common bombardier beetle, and both are rarely seen. B. sclopeta is so rare that it has only recently been accepted as a native species (past records were thought to be of rare migrants) and prior to 2005 had been presumed extinct since 1928. Because the beetles prefer habitats with thin soil, rubble and bare ground they tend to favour brownfield sites and have been found in east London; but with the continuous and unrelenting development of this area, these beetles’ futures are very precarious despite being listed as UK BAP priority species, and considered critically endangered by the IUCN. However, insect charity Buglife worked with developers to secure a site near London City Airport that is now the only known intact colony of the species in the UK. You can read Richard Jones highly informative blog about the relocation and conservation of this species.

Brachinus crepitans, though more common than B. sclopeta, is restricted to Southern England and Wales and especially the coastal areas of the South-East where it is considered nationally scarce. It is more commonly found in continental Europe, central Asia, the Middle East and North Africa, with central Sweden being the northernmost extreme of its range.

Brachinus crepitans. Image source: Wikipedia

Distribution of Brachinus crepitans. Source: NBN Gateway

Usually seen in May and June, the beetle favours calcareous grasslands, arable field margins and chalk quarries. It is usually found in dry, sunny areas – typically under stones. Little is known about its life-cycle, but it is thought that the larvae are external parasites on the pupae of other species of beetle, particularly those of the ground beetle Amara convexiuscula and a staphylinid beetle, Ocypus ater.

I think these gorgeous and enthralling beetles definitely warrant being surveyed for this coming Summer.

References:

Eisner, T. (2003) For Love of Insects. Harvard University Press, Cambridge Ma.
Lyneborg, L. (1976) Beetles in colour. Blandford Press, Dorset.
Bombardier beetle found near Honeybourne. Worcestershire Biological Records Centre (December 2015): http://www.wbrc.org.uk/WorcRecd/Issue11/BombBtle.htm
Isaak, M. 1997. Bombardier Beetles and the Argument of Design (December 2015):
http://www.talkorigins.org/faqs/bombardier.html
Streaked Bombardier Beetle. Buglife (December 2015) https://www.buglife.org.uk/campaigns-and-our-work/streaked-bombardier-beetle
Brachinus sclopeta UK Priority Species Data Collation. Joint Nature Conservation Committee. http://jncc.defra.gov.uk/_speciespages/2093.pdf

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

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.²

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.⁷Experimental 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

Timema cristinae, endemic to California has repeatedly evolved ecotypes adapted to different host plant species. One phenotype has no stripe and feeds on Ceanothus (left).

One ecotype features a distinct white stripe on its back and feeds on the thin, needle-like leaves of a shrub called Adenastoma.

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.⁴ 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).¹¹Although 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

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 sesquipedale, A. sororium and A. compactum and the evolution of extremely long spurs by pollinator shift’. Bot. Acta 110: 343-359