A 45-year examination of moose genetic diversity on Isle Royale

paper_in_a_nutshell

This nutshell is based on a recently published paper:

Decline of heterozygosity in a large but isolated population: a 45-year examination of moose genetic diversity on Isle Royale.  Renae L. Sattler, Janna R. Willoughby and Bradley J. Swanson. PeerJ 2017 5:e3584. (https://peerj.com/articles/3584.pdf)

 

 

Question: Should the loss of genetic diversity be a wildlife management concern for isolated populations?

We often think of a population’s health and long term viability in terms of its size, reproductive and survival rates. But a population’s genetic health is also an important component to ensure its existence into the future. Genetic diversity is the foundation for natural selection and thus its retention optimizes the ability of a population to adapt to a changing environment. And things are changing! In fact, populations with reduced genetic diversity can have lower reproductive performance and survival associated with increased inbreeding (Cassinello 2005; Marshall & Spalton 2006).

So how does a population maintain genetic variation? The easiest ecological process to facilitate the input of novel genetic material is the dispersal of animals between populations that successfully breed.

migration
Many animals travel considerable distances to disperse, migrate, and immigrate. This can provide novel genetic input into populations, and increase genetic diversity. 

But what happens if a population is isolated and can’t experience immigration from neighboring populations? How will its population’s genetic health change? To understand how changes in genetic variation occur over time in isolated populations, you not only need a closed population, but one with extensive demographic records and associated biological samples. Thus, we turned to Isle Royale, Michigan, an island located 23km from the nearest shore in Lake Superior.  Isle Royale is home to the longest running predator-prey study in the world: The Isle Royale wolf and moose study.

isleroyale
Isle Royale National Park, Michigan. The island is approximately 80 km long and 12 km wide, and is located in the northwestern portion of Lake Superior. At its shortest Euclidean distance, the island is 24 km off the southern coast of Canada (Sattler et al. 2017; https://peerj.com/articles/3584.pdf)

Moose colonized the island in the early 1900’s with just a few individuals. In 1959, Isle Royale researchers began collecting moose carcasses, which today has resulted in a store of greater than 4,500 carcasses spanning more than 50 years. For us, these carcasses held decades of resting genetic material and our chance to look back in time and reconstruct this population’s genetic health.

Just like your overall health is assessed using multiple measurements such as blood pressure, pulse rate, temperature and stress, genetic health is measured using several indices. The metrics we will be talking about here are the number of alleles, heterozygosity, inbreeding, and mitochondrial haplotype diversity. The number of alleles is literally the number of unique alleles at a loci (specific location on your DNA), where the more alleles the more potential genetic combinations.  Heterozygosity, as you may remember from genetic class, is having two different alleles at a loci. When this term is used in population genetics, it is referring to the prevalence of heterozygosity averaged across loci of sampled individuals and ranges 0 – 1, where higher values indicate higher genetic diversity.  Inbreeding is how closely related animals in a population are, and for our purposes is referred to as an inbreeding coefficient or FIS which is a measurement of how inbreed an individual is relative to the subpopulation (also averaged across loci and individuals).  FIS ranges from -1 to 1, where positive values represent individuals in a population are more related than you would expect under random mating and negative values indicate individuals are less related than you would expect under random mating.  Finally, mitochondrial haplotypes can be thought of as the number of female lineages in a population, where one lineage would mean a single female line has given rise to the population.

moose_skulls
DNA samples were collected from over 251 moose skulls and teeth dating back to 1960

To compare these indices of genetic diversity, we looked at these measures across 5 sampling periods: 1960-65, 1970-75, 1980-85, 1990-95, and 2000-05.  We selected 50-55 moose born within each sampling period and extracted DNA from residual tissue on the skull or from the pulp cavity of an extracted tooth.  All DNA samples (n=251) were amplified at 9 microsatellite loci and a subset of individuals (n=134) were sequenced at the mitochondrial control region.  First, we looked for evidence of immigration to the island to ensure the genetic history we find of the Isle Royale moose is representative of a closed system.  We did this by comparing the allele frequency distributions in each time period to simulated allele frequency distributions.  Additionally, we compared the number of haplotypes found on Isle Royale to those found in several North American Moose populations.  Second, we assessed the change in heterozygosity and inbreeding from 1960-2005.

What we learned

Neither our microsatellite derived allele frequencies nor mitochondrial lineages indicated any recent immigration into Isle Royale.  Our observed allele frequencies did not differ significantly from simulated allele frequencies.  We found a single mitochondrial haplotype on Isle Royale, which has also been found in moose populations in Minnesota, and North Dakota (Hundertmark et al. 2003). Since immigration from Minnesota or North Dakota seemed geographically unlikely, we did some digging and uncovered an anecdotal report that in 1907, 11-13 moose were translocated to Isle Royale from Minnesota (Peterson 1998).  How cool that evidence of how moose came to Isle Royale was hiding in genetic material over 100 years later!

figure1_moose.png
Figure 1: Comparison of heterozygosity between the empirical data from moose on Isle Royale and simulated Isle Royale moose populations. Empirical genetic diversity estimates are indicated by the solid line and reflect the mean heterozygosity for each of our five sampling periods. Simulated means are noted with the dashed line, and the 95% CI around the means are depicted with the grey band. From Sattler et al. 2017; https://peerj.com/articles/3584.pdf

When compared to neighboring Canadian mainland moose populations (where connectivity with neighboring populations is high), heterozygosity levels on Isle Royale were notably lower and FIS values higher (Wilson et al., 2003). The observed heterozygosity notably declined from 1960 to 2005 (p = 0.08, R2 = 0.70) and inbreeding coefficients approximately doubled from 0.08 in 1960–65 to 0.16 in 2000–05. The significant decrease in moose heterozygosity and increase in FIS values over our 45-year study period suggests that the moose population on Isle Royale was impacted by genetic drift and increased inbreeding, which is often associated with isolated populations.

Why is this important?

Habitat loss and landscape fragmentation resulting from increased anthropogenic impacts is on the rise.  It is increasingly likely that more wildlife populations will be facing the threats of loss of genetic diversity and accumulating inbreeding associated with small size and isolation preventing immigration that would bring new genetic material.  Our data support the notion that inbreeding is a significant force that acts to degrade heterozygosity over time, even in large and robust populations, in the face of isolation.  Therefore, in addition to demographic measurements of population health, managers need to consider a populations’ genetic health for long term population persistence.

Written by: Renae Sattler

References:

Cassinello J. 2005. Inbreeding depression on reproductive performance and survival in captive gazelles of great conservation value. Biological Conservation 122:453–464 DOI10.1016/j.biocon.2004.09.006.

Marshall TC, Spalton JA. 2006. Simultaneous inbreeding and outbreeding depression in reintroduced Arabian oryx. Animal Conservation 3:241–248.

Peterson B. 1998. The elusive origins of Isle Royale’s moose. The Moose Call 8:12–13.

Wilson PJ, Grewal S, Rodgers A, Rempel R, Saquet J, Hristienko H, Burrows F, Peterson R, White BN. 2003. Genetic variation and population structure of moose (Alces alces) at neutral and functional DNA loci. Canadian Journal of Zoology 81:670–683 DOI 10.1139/z03-030.

Photo credits:

Herd movement image: (c) GETTY IMAGES/MINT IMAGES RM

Walrus Image: http://www.nationalgeographic.com/photography/photo-of-the-day/2010/11/walruses-herd-svalbard/)

 

 

 

Leave a Reply

Fill in your details below or click an icon to log in:

WordPress.com Logo

You are commenting using your WordPress.com account. Log Out / Change )

Twitter picture

You are commenting using your Twitter account. Log Out / Change )

Facebook photo

You are commenting using your Facebook account. Log Out / Change )

Google+ photo

You are commenting using your Google+ account. Log Out / Change )

Connecting to %s