Module 8: Predator-Prey Coevolution & Conservation

Richard Dawkins and John Krebs (1979, Proceedings of the Royal Society B) articulated the evolutionary arms racemetaphor: coevolution between antagonists tends to produce escalating, costly adaptations on both sides. The driving asymmetry is the life-dinner principle: a prey faces stronger selection than its predator, because losing an encounter means death for the prey but only a missed meal for the predator.

Red Queen Hypothesis (Van Valen 1973)

Leigh Van Valen’s (1973) original article proposed the Red Queen hypothesisafter the Red Queen’s remark in Through the Looking-Glass: “It takes all the running you can do to stay in the same place.” Continuous adaptation is required just to maintain relative fitness. Van Valen’s original evidence was paleontological: extinction rates within taxa appeared constant over long intervals, implying the environment (dominated by biotic interactions) was continually deteriorating.

The formal model underlying Simulation 1 is a two-trait Lande-style response equation. Both traits escalate indefinitely under selection, constrained only by the quadratic cost of trait value.

Mimicry is one of the most visible outcomes of predator-prey coevolution. Two classical categories apply to aposematic (warning-signal) systems.

Batesian Mimicry

Henry W. Bates (1862) described tropical butterflies in the Amazon basin in which palatable species converged on the appearance of toxic, unpalatable species. The mimic gains protection from predators trained by the model species to associate the pattern with unpalatability. Classical examples: hoverflies (Syrphidae, harmless) resembling wasps; scarlet king snake (Lampropeltis elapsoides) resembling the highly venomous coral snake (Micrurus); the viceroy butterfly (Limenitis archippus) historically considered a Batesian mimic of the monarch (Danaus plexippus).

Müllerian Mimicry

Fritz Müller (1879) proposed that two or more unpalatable species converge on a common warning signal to share the cost of predator education. Classical examples: the Heliconius butterflies of the Neotropics, with\(\sim 30\) co-mimetic wing-pattern rings across Central and South America; Heliconius melpomeneand H. erato form the most extensively studied mimicry complex. Wing pattern is controlled by a handful of supergenes (optix, WntA, cortex) that co-segregate across species through introgression (the Heliconius Genome Consortium 2012, Nature).

Viceroy-Monarch Revisited

Ritland & Brower (1991) reassessed the textbook Batesian interpretation of the viceroy-monarch pair by feeding both species to naive birds: they found the viceroy is itself unpalatable, shifting the relationship toward Müllerian. The textbook example is thus a cautionary tale about distinguishing mimicry modes empirically.

The peppered moth (Biston betularia) is arguably the best-known case of rapid natural selection. Before the Industrial Revolution, the typical form (pale, speckled) dominated; by the late 19th century, the melanic carbonaria form had risen to\(>90\%\) in sooty British industrial towns. After clean-air legislation (UK 1956), the melanic form declined and the typical form recovered.

Kettlewell 1955: The Classic Experiment

Bernard Kettlewell’s (1955, 1956) mark-recapture experiments in Birmingham (polluted) and Dorset (unpolluted) demonstrated that the melanic form was preferentially predated on light birch in Dorset, whereas the typical form was preferentially predated on soot-darkened birch in Birmingham. Selection coefficient estimates were large (\(s \sim 0.2\)), consistent with the observed rapid allele-frequency change.

Cook 2012: Re-examination

Lawrence Cook, Bruce Grant, and colleagues (Cook et al. 2012, Biology Letters) re-analysed the evidence with improved statistics and replication. They strongly corroborated Kettlewell’s conclusion that bird predation on resting moths drove the polymorphism, and responded to methodological critiques. The genetic basis was identified as a single transposable-element insertion in the cortex gene (van’t Hof et al. 2016, Nature), dated to approximately 1819—aligning with the rise of industrial England.

Echolocating bats (Chiroptera) evolved ultrasonic sonar approximately 60 Mya. Moths, in response, evolved tympanic ears with threshold sensitivity tuned to the bat echolocation band (20–80 kHz). The tympanic organ in Noctuidae contains only two auditory neurons (A1 and A2); A1 fires at low SPL bat calls (distant bat), triggering directional evasive flight; A2 fires at high SPL (approaching bat), triggering power-dive reflexes (Roeder 1962; Hoy 1989).

Corcoran 2011: Moth-Generated Sonar Jamming

Aaron Corcoran and William Conner (2011, Science331:696) demonstrated a third tier: the tiger moth Bertholdia trigona emits its own 4500 ultrasonic clicks per second from specialised tymbal organs when approached by a hunting bat. Playback experiments with big brown bats (Eptesicus fuscus) showed a\(\sim\)10-fold drop in capture rate when the jamming signal was present. This is the first clear example of a prey directly interfering with a predator’s sonar.

Evolutionary Stable Strategy Analysis

The moth’s three-strategy space (silent, dive-ears, jamming) can be analysed as a two-player game against the bat’s two-strategy space (standard FM echolocation vs. stealth). Simulation 2 computes the Nash-ESS distribution by fictitious play. Depending on cost structure, the ESS tends toward a jamming-dominated equilibrium when jamming is cheap enough.

Ripple et al. (2014, Science 343:1241484) reviewed the status of the world’s 31 largest carnivores. 17 of 31 are in decline; 24 have had their ranges reduced by more than 50%. This finding synthesises the cross-link to M5 (Apex Predators, Trophic Cascades).

African Lion (Bauer 2015)

Bauer et al. (2015, PNAS 112:14894) analysed lion (Panthera leo) population trends across Africa and found a \(\sim 43\%\) decline in the monitored populations between 1993 and 2014, with the steepest losses in West and Central Africa. Only the four large southern African reserves showed stable or increasing populations. Conservative estimates placed the continental total at\(\sim 20{,}000\) lions in 2014, down from\(\sim 100{,}000\) in the 1960s.

Tiger: Poaching and Habitat

The tiger (Panthera tigris) occupies\(\sim 7\%\) of its historical range. Three of nine subspecies are extinct (Bali, Javan, Caspian). Tiger numbers hit a low of \(\sim 3{,}200\) in 2010 but have since recovered to\(\sim 4{,}000\)–\(5{,}000\)globally, largely driven by Indian reserves (Ranthambore, Bandhavgarh, Kaziranga, Sundarbans) and Russian Amur tiger stabilisation. Poaching for traditional medicine markets in East Asia remains the dominant human mortality.

Southern Resident Killer Whale

The southern resident killer whale (SRKW) population, three matrilines off the Washington-Vancouver coast, has declined from 98 individuals in 1995 to fewer than 75 today. Drivers include: (1) decline of their preferred Chinook salmon prey; (2) persistent organic pollutants including PCBs bioaccumulating in blubber at among the highest body burdens measured in any marine mammal; (3) acoustic disturbance from shipping traffic (Lacy et al. 2017 Scientific Reports); and (4) small-population genetic inbreeding. A proposed oil pipeline from Alberta to coastal BC would increase tanker traffic and oil-spill risk through SRKW habitat.

Dingo and Mesopredator Release

Australian continental removal of the dingo (Canis dingo) within the Dingo Fence zone has allowed introduced red fox (Vulpes vulpes) and feral cat populations to expand, with devastating consequences for native small mammals. Australia has lost more than 30 mammal species since European colonisation—the highest rate of mammalian extinction on any continent. Letnic et al. (2012) and Ritchie & Johnson (2009) established that restoring dingo populations suppresses mesopredators and benefits native prey.

The Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) entered into force in 1975 and today regulates trade in \(\sim 38{,}700\) species through three Appendices. Appendix I prohibits commercial trade; Appendix II requires CITES-compliant export permits; Appendix III allows unilateral listing by range states. Tigers, snow leopards, orang-utans, great white sharks, and all elephant species are Appendix I.

IUCN Red List

The IUCN Red List classifies taxa into categories from Least Concern (LC) to Extinct (EX), with four threatened categories in between (Vulnerable VU, Endangered EN, Critically Endangered CR). Criteria include range size, population size, rate of decline, and fragmentation. For a species to qualify as Vulnerable under criterion A, a\(\geq 30\%\) decline over three generations suffices. The African lion is assessed as VU, the tiger EN, the Iberian lynx CR (recently downlisted to EN following recovery), and the Yangtze finless porpoise CR.

Endangered Species Act (USA 1973)

The US Endangered Species Act (ESA) requires federal agencies to consult on any action that may “jeopardize the continued existence” of listed species or “adversely modify critical habitat.” The grey wolf (Canis lupus), peregrine falcon (Falco peregrinus), bald eagle, and American alligator are ESA recovery success stories; wolves were delisted from the northern Rocky Mountain range in 2011, though litigation has cycled their status since.

Trophy Hunting (Lindsey 2019)

Lindsey et al. (2019, Conservation Biology) reviewed the evidence on trophy hunting of large carnivores. The practice generates revenue but is controversial: proponents argue it funds habitat retention and anti-poaching; critics argue it preferentially removes reproductively valuable males, generates infanticide cascades in lions (Loveridge 2007), and relies on opaque governance. Lindsey’s analysis concluded that moratoria generally reduce overall conservation funding without clear ecological benefit unless accompanied by substitute revenue streams.

Large carnivores coexist with humans in pastoral landscapes at the cost of livestock depredation and, occasionally, direct human attacks. Mitigation strategies include:

• Livestock guardian dogs— Turkish Kangal, Anatolian shepherd, Great Pyrenees; reduce leopard, lion, and coyote depredation by 60–90% (Rigg et al. 2011).
• Predator-proof kraals/bomas— reinforced night enclosures; African lion depredation drops\(>70\%\) (Lichtenfeld et al. 2015).
• Compensation schemes— verified livestock losses compensated by government or NGO funds (snow leopard in Nepal/Pakistan; wolf in Scandinavia).
• Conditioned taste aversion— laced baits induce aversion to specific prey species (lithium chloride-baited coyote experiments; Gustavson 1974).
• Fladry and fencing— rope flag-lines and predator-exclusion fencing; mixed efficacy.

• Grey wolf reintroduction— 1995 Yellowstone reintroduction (see M5); 2000s–present European recolonisation of Germany, Netherlands, Belgium, France, Denmark (Chapron et al. 2014 Science).
• Peregrine falcon— near-extirpation from DDT-induced eggshell thinning; captive-breeding and release plus DDT ban (1972 USA) restored populations to 17\(,\)000 pairs in North America by 2000; delisted 1999.
• California condor(Gymnogyps californianus) — reduced to 22 individuals in 1987; all captured; captive breeding plus lead-ammunition phase-out (2019 California statewide) brought wild population to over 300 birds.
• Iberian lynx(Lynx pardinus) — 100 individuals in 2002 in Spain and Portugal; captive-breeding plus reintroduction plus European rabbit (Oryctolagus cuniculus) recovery programs brought population to\(>2{,}000\) by 2024.
• Giant panda(Ailuropoda melanoleuca) — downlisted from Endangered to Vulnerable in 2016 (IUCN); now\(\sim 1{,}800\) wild adults; reserve network and bamboo forest protection.
• Amur leopard— fewer than 40 individuals in 2007; Russian Land of the Leopard National Park (2012) protected key habitat; now \(\sim 120\) individuals.
• Black-footed ferret(Mustela nigripes) — declared extinct 1979; rediscovered 1981 Wyoming; captive-breeding plus sylvatic plague vaccination of prairie dog colonies restored wild population.

Genetic Rescue

Small populations suffer inbreeding depression; introducing a small number of migrants from a genetically diverse source population can reverse fitness declines. Florida panther (Puma concolor coryi) received 8 Texas cougar females in 1995; cub survival and body condition rebounded measurably within a generation (Johnson et al. 2010 Science). Similar strategies are under consideration for mountain lion populations in California and for isolated wolf populations.

Rewilding

Rewilding is the large-scale restoration of ecosystems and predator-prey dynamics through reintroduction of keystone species and passive habitat recovery. European projects include the reintroduction of European bison (Bison bonasus) to Romania, Poland, and Germany; the Oostvaardersplassen experiment in the Netherlands (ca. 1983–2018); and Knepp Estate rewilding in England (Tree 2018). North American rewilding includes the Yellowstone-to-Yukon corridor concept and American Prairie Reserve in Montana.

• Newt-snake tetrodotoxin arms race— Taricha granulosa (rough-skinned newt) evolved extreme tetrodotoxin loads; sympatric Thamnophis sirtalis garter snakes evolved point-mutations in Na\(_V\)1.4 channel conferring resistance (Brodie & Brodie 1991 onward).
• Cuckoo-host egg mimicry— brood parasitism by Cuculus canorus induces host egg-pattern evolution; hosts discriminate foreign eggs, cuckoos match host patterns in escalating reciprocal selection (Stoddard 2012 Science).
• Rough-skinned newt-garter snake arms race (eastern US)— geographic mosaic coevolution (Thompson 2005); toxin and resistance levels vary across sympatric populations and decouple where allopatric.
• Escape-and-radiate(Ehrlich & Raven 1964)—plants escape herbivores through novel chemical defences, then radiate; herbivores evolve counter-defences and radiate in turn, producing coupled diversification.
• Thomson 1994 Geographic Mosaic Theory— coevolution varies in intensity and direction across geography, producing hot and cold spots; local trait matching does not imply global coevolution.
• Clay-Kondrashov Red Queen for sex— the Red Queen provides a leading hypothesis for the maintenance of sexual reproduction: rapid recombinatorial evolution keeps pace with parasites better than clonal lineages (Hamilton 1980; Lively 1987 New Zealand mud snail Potamopyrgus).
• Wolf-moose Isle Royale— world’s longest continuous predator-prey study, 1958–present (Vucetich & Peterson); founder genetic rescue by a mainland male in 1997 rescued a collapsing wolf population, subsequently reversed by intra-pack disease.