Gabriel Shields-Estrada

Professor Bill Durham

Darwin, Evolution, and Galapagos

13 October 2008

Disease Susceptibility in Endemic Species:

a case study in the Galapagos Hawk

ABSTRACT

In this paper I seek to illustrate disease susceptibility in endemic species through an

analysis of the Galapagos hawk. I provide a brief introduction to the Galapagos hawk

(Buteo galapagoensis) and describe important characteristics of the bird. I introduce

three hypotheses that I seek to address in this paper: (1) small populations of endemic

birds have less genetic variation than non-endemic birds (2) lack of genetic variation in

endemics increases the risk for disease compared to non-endemic species (3) new risks of

invasive disease have arisen as a result of economic growth and development. I address

each hypothesis in turn. First, I establish the lack of genetic variation in the Galapagos

hawk. Second, I use a comparison of incidence of ectoparasites between the Galapagos

hawk and its closest non-endemic relative to establish increased disease susceptibility.

Lastly, I establish the positive correlation between increased economic development and

risk of disease. I finish with specific recommendations for feasible policies to eliminate

these risks.

BACKROUND

The Galapagos hawk is a large hawk endemic to the Galapagos Islands. Its range

includes Santa Fe, Española, Pinzón, Santiago, Isabela, Fernandina, Pinta, and Marchena

islands. The hawk is one of the foremost predators on the archipelago and measures

approximately 55cm from beak tail with a wingspan of 120cm. The Galapagos Hawk is

also polyandrous. It is an especially good model for endemic species because of its small

population size, estimated to be 300 adults (http://www.hawk-conservancy.org/priors/

galapagoshawk.shtml), and high rate of inbreeding, both of which are traits common to

endemic populations.

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GENETIC VARIATION

Genetic variation is one of the most important pieces of any species’ survival

mechanism. Diversity of genes across a population allows a species to survive

environmental changes, whether that come in the form of climate change, habitat

destruction, or disease introduction. For example, having a diversity of genes that control

for body size may allow a species to survive in times of famine. Similarly, lack of

genetic variation in genes that control the immune system will provide an immune

response that is less able to handle introduced diseases. In order to test my hypothesis

that small populations of endemic birds have less genetic variation than non-endemic

birds, I analyzed recent genetic research performed on the Galapagos hawk.

Methodology

In a recent study entitled Population Genetics of the Galapagos Hawk (Buteo

galapagoensis): Genetic Monomorphism within Isolated Populations by Jennifer

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Bollmer, Noah Whiteman, et al. and conducted in 2005, the researchers analyzed FST

values to compare genetic variation across species. They began by drawing blood

samples from nine populations of Galapagos Hawks (the ninth population was from Santa

Cruz Island and is thought to have been juveniles who had flown there). They then used

genetic fingerprinting to identify 14 genes of interest. These areas of focus were

“multilocus minisatellite DNA markers” (Bollmer et al. 2005, 3), which are

“hypervariable” regions in DNA. In other words, the researchers used a very

conservative estimate of genetic variation by looking at the similarities between highly

variable areas of DNA. After identifying the genes, the researchers ran a fingerprinting

gel of the multilocus minisatellite DNA. Ultimately, the researchers hoped to establish a

positive correlation between population size and genetic variation.

Results

The results of their study were as follows:

Figure 1

ISLAND WITHIN ISLAND

FST

Pinzon 0.903

Santa Fe 0.956

Pinta 0.765

Espanola 0.900

Marchena 0.891

Santiago 0.711

Fernandina 0.719

Santa Cruz 0.657

Isabela 0.693

(Bollmer et. al. 2005: 6)

FST values (measure of the similarity across genes ranging between 0 and 1) for the

Galapagos hawk appeared substantially higher than non-endemic bird populations. In

Non-endemic bird

populations:

0.2—0.3

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addition, the FST value across the islands is 0.617 (Bollmer et al. 2005: 6), suggesting

extreme genetic similarity not only within but also across populations of the Galapagos

hawk. FST values are 200 to 400% the standard value for non-endemic species. A linear

regression run correlating total island area (the stand in value for population size) with

genetic variation resulted in r = 0.844 and P = 0.008. The extremely high r value tells us

that 84.4% of all genetic variation can be explained directly by population size. The P

value of 0.008 adds to the evidence by demonstrating that the correlation is very

significant (P 0.5).

Conclusions

The FST values among the Galapagos hawks are 200-400% those of non-endemic

species and therefore it can be concluded that the hawk has much more genetic similarity

both within and across populations. They have the “highest reported levels of

monomorphism at minisatellite loci of any natural bird population” (Bollmer et al. 2005:

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8). This incredibly high correlation (FST =0.617) across Galapagos hawks is evidence of

a single founder event and lack of selective pressures on the different populations

(Bollmer et. al. 2005: 8). But the even higher FST values among individual populations

are evidence of little to no mixing across islands. This is also consistent with the

behavior of the Galapagos hawk’s closest relative (Swainson’s hawk) on the mainland,

which does not like to fly across water. Because endemic species usually have smaller

populations than their non-endemic counterparts, we can use the strong positive

correlation between island size (population size) and lack of genetic variation to conclude

that endemic species have less genetic variation than non-endemics. Further evidence of

this is provided by analysis of geographic distance and FST values, which reveal that

increasing geographic distance between islands results in greater genetic variation

(Bollmer et al. 2005: 10). Ultimately, I conclude that this evidence supports my

hypothesis that endemic birds have less genetic variation than non-endemic birds.

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DISEASE SUSCEPTIBILITY

To establish the correlation between this lack of genetic variation and disease

susceptibility in endemic species I will analyze the incidence of ecto-parasites on the

Galapagos hawk and it’s closest relative in the Americas, the Swainson’s hawk.

Although ecto-parasites are admittedly not a disease of the viral or bacterial type, they do

indeed provide evidence of immune defenses and the accordant disease susceptibility. To

especially emphasize this point, I will look at research that analyzes two types of

parasites, one that comes in contact with the immune system, and one that doesn’t.

Through this research I will test my hypothesis that lack of genetic variation in endemics

increases the risk for disease compared to non-endemic species.

Methodology

Researchers Noah Whiteman, Kevin Maton, et al. conducted a study in 2005

entitled Disease ecology in the Galapagos Hawk: host genetic diversity, parasite load,

and natural antibodies. In the study they analyzed two quantitative variables: natural

antibody (NAb) levels and ectoparasite levels. The two ectoparasites in the study were

amblyceran lice, which encounters the host’s immune system, and ischnoceran, which

does not. The researchers quantified the number of lice and NAb levels for both the

Galapagos hawk and Swainson’s hawk in order to compare the endemic with the non-

endemic species.

Results

In the Galapagos hawk there was a negative correlation between both amblyceran

louse and ischnoceran abundance and genetic variation. For the amblyceran louse, r = -

0.949, and p = 0.0001 (Whiteman et al. 2006: 802). For the ischnoceran, r = -0.854 and p

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= 0.01 (Whiteman et al. 2006: 802). In both cases the r values are very strong; genetic

variation explains 94.9% and 85.4% of ectoparasite abundance respectively. P values for

both also provide evidence of highly significant correlations. Researchers found a similar

result with NAb levels. Although the r value was not provided, there was a negative

correlation between NAb agglutination titres and amblyceran louse abundance with p =

0.01. This p value is again evidence of a significant correlation. There was no

correlation between NAb titres and ischnoceran, which is expected because the

ischnoceran does not come in to contact with the host immune system (Whiteman et al.

2006: 802). A comparison of quantitative values between the Galapagos hawk and

Swainson’s hawk can be found below:

Galapagos Hawk Swainson’s Hawk

Amblyceran louse 75 2

Ischnoceran 14 2

(Whiteman et al. 2006: 801)

This raw data illustrates the correlation between genetic variation and increased incidence

of ectoparasites convincingly. Swainson’s hawks have much greater genetic variation

and, as would be predicted by the correlation, many fewer parasites. Although the raw

data is not provided for the NAb agglutination titres, the r values increases in correlation

strength from r= -0.875 to r = -0.949 with the addition of the data from Swainson’s

hawks. This is evidence for these hawks fitting the model of negative correlation

between genetic variation and incidence of ectoparasites.

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Conclusions

Based on the much higher incidence of parasites in the endemic Galapagos hawk

compared to the non-endemic Swainson’s hawk, and the strong negative correlation

between genetic variation and incidence of parasites, we can conclude that lack of genetic

variation equates with higher parasite loads as a result of “lower variation in within-

population immune response” (Whiteman et al. 2006: 803). Similarly, from strong

negative correlations between NAb agglutination titres and incidence of parasites we can

conclude that lower NAb levels equate with higher parasite loads (Whiteman et. al. 2006:

803). From the first section of this paper we know that endemic populations have a lack

of genetic variation. Therefore, we can conclude that endemic species, which have a lack

of genetic variation, also have lower NAb levels and a higher parasite load. Ultimately,

this parasite load can be seen as a model for disease, which like the amblyceran louse,

comes in contact with the host’s immune system. This leads us to the inference that

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Galapagos hawks have a higher susceptibility to disease because of their lack of genetic

variation (Whiteman et al. 2006: 803). I acknowledge that this correlation does not

equate with causation, but in this case, such causation is both highly plausible and

probable. Similar conclusions have been made with regard to gazelles (Cassinello J et al.

2001: 1173) and Soay sheep (Coltman D et al. 1999: 1265) Therefore, I will assume that

such lack of genetic variation is the cause of disease susceptibility and conclude that this

is evidence supporting my hypothesis that endemic species are more susceptible to

disease than non-endemics because of their lack of genetic variation. Evolutionarily, this

disease susceptibility is increasingly problematic for the Galapagos hawk because the

lack of variation among genes precludes rapid adaptation to emerging challenges and

diseases.

NEW RISKS

With the advent of twenty-first century globalization, these challenges are

appearing at a rapid rate. Increases in agriculture, livestock, and tourism in the

Galapagos present many new issues. I hypothesize that introduced species and increased

travel have led directly to the introduction of invasive disease.

Already, introduced avipox and avian malaria have been found in endemic birds.

Cases of avipox have been identified in mockingbirds, doves, warblers, and finches

(Thiel et al. 2005: 343) and avian malaria has been documented in penguins. The vectors

for West Nile and Newcastle disease have been found in the Galapagos (Whiteman et al.

2005: 845), so the arrival of an infected bird or other organism will lead to the rapid

spread of the invasive disease. In addition, fears of recombination and mutations are

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high. One of the largest problems currently is chickens. Poultry are raised both in

backyards and in broiler houses. Both present major problems for endemic birds.

Chickens raised in backyards come into close contact with finches, mockingbirds, and

warblers as they search for food among the underbrush (Gottdenker et al. 2005: 436).

Yet perhaps even more dangerous, broiler houses with chickens in close contact allow for

close genetic overlap in disease serotypes, a perfect situation for mutations and increased

virulence (Gottdenker et al. 2005: 436). This evidence supports my hypothesis that

increased economic development is leading to increased incidence of invasive disease

and has the potential to lead to more introductions and diseases. It’s easy to proclaim that

we should just shut down all poultry operations and any other practices that spread

disease, but it’s imperative to remember that these chicken, along with many other

cultural practices, are part of the local economy and critical to the needs of citizens. But

before proceeding to recommendations, it is important to ask whether these diseases do

indeed pose a problem to the Galapagos hawk and other predatory birds, or only to

herbivorous and insectivorous birds. And indeed they do. Recent analyses in Hawaii and

the Americas have found worrisome results. In Hawaii, similar infections (avipoxvirus)

have been found in herbivorous/insectivorous birds and it is expected that the virus will

make the jump to predatory birds in the next few years (Thiel et al. 2005: 342). In the

Americas, avipox virus infections have been found in both the rough-legged hawk in

North Dakota (Buteo lagopus) (Pearson et al. 1975: 224) and in Swainson’s hawk (Buteo

swainsoni) (Miller D.S. et al. 2004: 400). Undoubtedly, invasive diseases, both current

and projected, pose a real threat to the Galapagos hawk.

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CONCLUSIONS & RECOMMENDATIONS

The most critical piece of this danger is the lack of genetic variation in the

Galapagos hawk that makes it susceptible to disease. Galapagos hawk FST values are

200-400% of standard non-endemic birds like the Swainson’s hawk, convincingly

illustrating this lack of genetic variation. In addition, the Galapagos hawk has a much

higher parasite load, and the correlation between genetic variation and parasite load is

strongly negative. This is further of evidence of lack of genetic variation correlating with

increased susceptibility to disease. Although this lack of genetic variation cannot be

proven to be the cause of increased disease susceptibility, the correlation is strong and

cause can be concluded to be probable (Spielman D. et al. 2005: 439). Regardless, the

Galapagos hawk faces serious challenges with new economic development and 21st

century globalization taking place in the Galapagos. Without even mediocre genetic

variation the Galapagos hawk will remain highly susceptible to invasive disease, because

the extreme similarity across hawks will make them all susceptible to the same diseases,

thus putting them at risk for extinction. As their environment changes rapidly, they

simply will not be able to adjust evolutionarily to the new selective pressures. Therefore,

we must act to stop this change in the hawks’ environment by limiting the spread of

introduced and invasive disease.

The most effective measures are those that are simple, feasible, and do not hurt

local citizens financially. Perhaps the most easily implemented policies are those that

will minimize contact between native and introduced animals, and domestic and wild

animals. Although a bit more involved, rules that mandate controls, inspections, and

sprays will be highly effective for eliminating both diseases and their vectors, delivering

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a one-two punch to invasive species and diseases. Ultimately, this culminates in two

simple policies that will have profound impacts: (1) spraying planes either during flight

or immediately upon arrival to the Galapagos and (2) caging domestic fowl and other

introduced animals. These control measures will have a profound impact on limiting the

number of invasive diseases with the potential to reach the Galapagos hawk. Even with

their lack of genetic variation and increased susceptibility to disease, the hawk will

survive if we can effectively implement these policies. On a wider scale, it is possible

that similar policies on other islands will effectively insulate endemic species from their

respective disease threats. Endemics the world over face the challenge of surviving rapid

environmental change with limited to minimal genetic variation. It is our responsibility

to rectify the environmental changes we have caused by working to preserve these

species.

QuickTime™ and aTIFF (Uncompressed) decompressor

are needed to see this picture.

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Works Cited

Bollmer, J. L., Whiteman, N. K., Bednarz, J. C., DeVries, Tj. & Parker, P. G. In press a

Population genetics of the Galápagos hawk: genetic monomorphism within

isolated populations. Auk.

Cassinello J, Gomendio M, Roldan E.R.S. Relationship between coefficient of inbreeding

and parasite burden in endangered gazelles. Conserv. Biol. 2001;15:1171–1174.

Coltman D.W, Pilkington J.G, Smith J.A, Pemberton J. Parasite-mediated selection

against inbred Soay sheep in a free-living, island population. Evolution.

1999;53:1259–1267.

Gottdenker Nicole L., Walsh Timothy, Vargas, Hernan et al. Assessing the risks of

introduced chickens and their pathogens to native birds in the Galapagos

Archipelago. Biological Conservation. 2005; 126: 429-439.

Miller D.S., Taton-Allen G.F., Campbell T.W. Knemidokoptes in a Swainson’s Hawk,

Buteo Swainsoni. J Zoo Wildl Med. 2004; 35; 400-402.

Spielman D, Brook B.W, Briscoe D.A, Frankham R. Does inbreeding and loss of genetic

diversity decrease disease resistance? Conserv. Genet. 2004b;5:439–448.

Thiel T, Whiteman N.K, Tirapé A, Baquero M.I, Cendeño V, Walsh T, Uzcátequi G.J,

Parker P.G. Characterization of canarypox-like viruses infecting the endemic

birds in the Galápagos Islands. J. Wildl. Dis. 2005;41:342–353. [PubMed]

Whiteman N.K, Goodman S.J, Sinclair B.J, Walsh T, Cunningham A.A, Kramer L.D,

Parker P.G. Establishment of the avian disease vector Culex quinquefasciatus

Say, 1823 (Diptera: Culicidae) on the Galápagos Islands, Ecuador. Ibis.

2005;147:844–847.

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Whiteman, N.K. et.al. Disease ecology in the Galápagos Hawk: (Buteo galapagoensis):

host genetic diversity, parasite load, and natural antibodies. Proceedings of the

Royal Society: Biological Sciences. 7 April 2006.

http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1560217

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Works Consulted

de Castro F, Bolker B. Mechanisms of disease-induced extinction. Ecol. Lett.

2005;8:117–126.

Frankham R. Inbreeding and extinction: island populations. Conserv. Biol. 1998;12:665–

675.

Reid, W.V.; Miller, K.R. World Resources Institute; Washington, DC: 1989. Keeping

options alive: the scientific basis for conserving biodiversity

Wikelski M, Foufopoulos J, Vargas H, Snell H. Galápagos birds and diseases: Invasive

pathogens as threats for island species. Ecol. Soc. 2004;9

http://www.ecologyandsociety.org/vol9/iss1/art5

Taylor, J.E. et.al. Economics of ecotourism: A Galápagos Islands Economy-Wide

Perspective. Economic Development and Cultural Change. 51: 977-997, July

2003.