Patterns of Genetic Diversity and Its Loss in
Mammalian Populations
ALISSE GARNER, JANET L. RACHLOW,∗ AND JASON F. HICKS
Department of Fish and Wildlife Resources, University of Idaho, Moscow, ID 83844, U.S.A.
Abstract: Policy aimed at conserving biodiversity has focused on species diversity. Loss of genetic diversity,
however, can affect population persistence, evolutionary potential, and individual fitness. Although mammals
are a well-studied taxonomic group, a comprehensive assessment of mammalian genetic diversity based on
modern molecular markers is lacking. We examined published microsatellite data from populations of 108
mammalian species to evaluate background patterns of genetic variability across taxa and body masses. We
tested for loss of genetic diversity at the population level by asking whether populations that experienced demographic threats exhibited lower levels of genetic diversity. We also evaluated the effect of ascertainment bias
(a reduction in variability when microsatellite primers are transferred across species) on our assessment of
genetic diversity. Heterozygosity did not vary with body mass across species ranging in size from shrews to
whales. Differences across taxonomic groupings were noted at the highest level, between populations of marsupial and placental mammals. We documented consistently lower heterozygosity, however, in populations
that had experienced demographic threats across a wide range of mammalian species. We also documented a
significant (p = 0.01) reduction in heterozygosity as a result of ascertainment bias. Our results suggest that
populations of both rare and common mammals are currently losing genetic diversity and that conservation
efforts focused above the population level may fail to protect the breadth of persisting genetic diversity. Conservation policy makers may need to focus their efforts below the species level to stem further losses of genetic
resources.
Key Words: ascertainment bias, body mass, conservation policy, genetic variability, mammalia, mammals, microsatellites, threatened populations
Patrones de Diversidad Genética y su Pérdida en Poblaciones de Mamı́feros
Resumen: Las polı́ticas de conservación de la biodiversidad tradicionalmente se han centrado en la diversidad de especies. Sin embargo, la pérdida de diversidad genética puede impactar al potencial de persistencia
y evolutivo, ası́ como a la adaptabilidad individual. Aunque los mamı́feros son un grupo taxonómico bien
estudiado, se carece de una evaluación integral de la diversidad genética de mamı́feros basada en marcadores
moleculares. Examinamos datos publicados de microsatélites de poblaciones de 108 especies de mamı́feros para
evaluar los patrones de variabilidad genética entre los taxa y masas corporales. Probamos la pérdida de variabilidad en el nivel poblacional preguntando si las poblaciones que experimentaron amenazas demográficas
exhibieron menores niveles de diversidad genética. También evaluamos el impacto del sesgo de determinación
(una reducción en la variabilidad cuando los iniciadores de microsatélites son transferidos a otras especies)
sobre nuestro análisis de diversidad genética. La heterocigosidad no varió con la masa corporal en especies que
variaron en tamaño desde musarañas hasta ballenas. Las diferencias entre grupos taxonómicos se notaron en
el nivel más alto, entre poblaciones mamı́feros marsupiales y placentarios. Sin embargo, en un amplio rango
de especies de mamı́feros consistentemente documentamos menor heterocigosidad en poblaciones que habı́an
experimentado amenazas demográficas. También documentamos una reducción significativa (p = 0.01) en
la heterocigosidad como resultado del sesgo de determinación. Nuestros resultados sugieren que poblaciones
∗ Address
correspondence to J.L. Rachlow, email [email protected].
Paper submitted January 20, 2004; revised manuscript accepted August 26, 2004.
1215
Conservation Biology 1215–1221
C 2005 Society for Conservation Biology
DOI: 10.1111/j.1523-1739.2005.00105.x
1216
Mammalian Genetic Diversity
Garner et al.
de mamı́feros, tanto raras como comunes, están perdiendo diversidad genética actualmente y que los esfuerzos de conservación por encima del nivel de población pueden fallar en la protección de la amplitud de la
diversidad genética persistente. Puede ser necesario que la definición de polı́ticas de conservación enfoque sus
esfuerzos por debajo del nivel de especie para evitar mayores pérdidas de recursos genéticos.
Palabras Clave: mamı́feros, mammalia, masa corporal,microsatélites, poblaciones amenazadas, polı́ticas de conservación, tendencia de averiguación, variabilidad genética
Introduction
Conservation policy usually focuses on maintaining species-level biodiversity. Genetic diversity, however, which
is the variation of alleles and genotypes within a population (Frankham et al. 2002), provides the foundation
for adaptation and evolutionary potential. An inventory
of current biodiversity, including genetic diversity, is necessary for quantifying variability, evaluating losses, and
gauging success of conservation efforts. An understanding of patterns of biodiversity loss should improve policy
decisions aimed at stemming the degradation of biological resources (Raven & Wilson 1992; Groves et al. 2002).
Loss of genetic diversity has several potential consequences. Theoretical studies suggest that genetically depauperate populations have reduced abilities to adapt to
environmental changes (Hoffmann & Parsons 1997) and
higher probabilities of extinction (Mills & Smouse 1994;
Lacy 1997; Frankham et al. 2002). Studies linking genetic
diversity to both individual fitness and population persistence (Coltman et al. 1999; Hansson & Westerberg 2002;
Reed & Frankham 2003) underscore the importance of
conserving the breadth of existing genetic variability. Indeed, the World Conservation Union (IUCN) recognizes
maintenance of genetic diversity as one of three global
conservation priorities (McNeely et al. 1990).
Techniques for measuring genetic diversity have advanced over the past several decades. Initial genetic research focused on allozymes, polymorphic enzymes detected with electrophoresis. In recent years, microsatellites, which are regions of short tandem repeats of one
to six nucleotide base pairs, have replaced allozymes as
genetic markers commonly used to investigate diversity
(Haig 1998; Hedrick 1999). Despite their selective neutrality, microsatellites are thought to represent an appropriate surrogate for adaptive genetic diversity. Heterozygosity of neutral markers (such as microsatellites) is expected to be positively correlated with fitness either because microsatellite loci are linked to important loci under selection or because microsatellite diversity reflects
genome-wide diversity (Hansson & Westerberg 2002; but
see Reed & Frankham 2003). Because microsatellites have
higher mutation rates than protein-coding genes and are
hypervariable (Haymer 1994), they provide a measure of
genetic variability on a finer scale than allozymes (Hughes
& Queller 1993; Schlötterer & Pemberton 1994).
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Volume 19, No. 4, August 2005
Two common measures of genetic variation include
multilocus heterozygosity, which reflects the proportion
of heterozygotes within a population, and mean number
of alleles per locus, which represents the diversity of alleles at each locus within a population. Because heterozygosity is less likely than allelic diversity to be influenced
by variation in sample sizes (Leberg 2002) or geographic
range over which samples are collected, heterozygosity is
often used as a measure for contrasting genetic diversity
across studies. Because of the expense and time required
to develop novel microsatellite primers, existing primers
are often transferred across species, genera, and even families. Primers designed for a particular species may be less
variable, however, when applied to other species, a phenomenon known as “ascertainment bias” (Primmer et al.
1996; Webster et al. 2002). The extent of this bias is largely
unknown but may have substantial effects on assessments
of genetic diversity across species.
Although mammals are among the most studied and
least diverse classes of organisms, a comprehensive assessment of mammalian genetic diversity based on microsatellite markers is lacking. Previous reviews of genetic diversity in mammals assessed patterns of allozyme
diversity across species as a function of body mass, which
serves as a useful surrogate for a suite of life-history traits
(Eisenberg 1981). Those studies postulated that largerbodied species exhibit lower levels of genetic diversity
(Selander & Kaufman 1973; Wooten & Smith 1985) or alternatively that diversity is uniform across body masses
(Baccus et al. 1983) and mammalian species (Makarieva
2001). Knowledge of potential background patterns of
genetic variability, such as the correlation between body
mass and heterozygosity, provides a context for examining loss of genetic diversity in mammals.
Losses of mammalian diversity have been noted at the
species, population, and individual levels. The IUCN Red
List, which is a global benchmark for species-level diversity, places 24% of mammalian species in the three
highest threat categories ( World Conservation Union,
http://www.redlist.org). At the population level, recent
research has indicated that mammalian populations have
been extirpated over roughly half of their historical ranges
(Ceballos & Ehrlich 2002). Many mammalian populations
are genetically depauperate as well (Gottelli et al. 1994;
Driscoll et al. 2002; Frankham et al. 2002). The extent
to which genetic diversity has been lost across the class,
Garner et al.
however, is unknown. Several demographic factors may
reduce levels of genetic diversity within populations, including declines in population size, bottlenecks, range
reductions, and isolation from conspecifics (Gibbs 2001;
Frankham et al. 2002; England et al. 2003). Although various researchers have used microsatellite markers to examine the impact of these factors on populations of mammals, a comprehensive assessment of microsatellite diversity across the class is lacking.
We reviewed studies that applied microsatellite analyses to mammalian populations across a diverse array of
species. We evaluated background patterns of heterozygosity across body masses and taxonomic groupings. We
then assessed loss of diversity by testing the hypothesis
that populations that have experienced a demographic
threat exhibit lower levels of genetic variation than do
populations without a history of demographic threats.
Lastly, we evaluated the effect of ascertainment bias on
assessments of genetic diversity. This study synthesizes
genetic data across mammalian species, and our results
can help researchers evaluate patterns of genetic diversity and its loss at the population level.
Methods
We examined microsatellite data from peer-reviewed literature to evaluate current patterns of genetic diversity in
populations of mammals (detailed table available from authors upon request). We reviewed all issues of six journals
(Animal Conservation, Conservation Biology, Conservation Genetics, Heredity, Journal of Mammalogy, and
Molecular Ecology) from January 1990 to August 2002.
Other sources included selected primer notes from Molecular Ecology, papers located through literature searches,
and original papers listed in recent key articles (Goossens
et al. 2001; Neff & Gross 2001; Walker et al. 2001; Bowyer
et al. 2002). Studies with fewer than five microsatellite
loci or with sample sizes smaller than an average of 10
individuals per population were excluded. We also excluded studies of domestic species or captive populations. Data from 130 papers and 108 species were included in the analyses. Information recorded from each
included number of microsatellite loci, observed and expected heterozygosities, sample size, number of populations sampled, and population history. When microsatellite loci were reported as being out of Hardy-Weinberg
equilibrium, those loci were excluded and heterozygosity
values were recalculated. We used expected heterozygosity in most cases, but because observed heterozygosity
will be close to expected in most outbreeding populations (Hedrick 2000), observed heterozygosity was used
when expected was not reported.
We evaluated the demographic history of each population included in this synthesis. Demographic factors that
Mammalian Genetic Diversity
1217
may influence persistence of genetic diversity include
population declines, bottlenecks, reduction of population range, and isolation from conspecifics (Gibbs 2001;
Frankham et al. 2002; England et al. 2003). These same
demographic factors are used by the IUCN in assessing
risk of extinction for species on the IUCN Red List (IUCN
2001). Although authors of the genetic studies often did
not provide information necessary to quantify risk level
according to the IUCN criteria, we used the information
provided in the published studies to qualitatively evaluate whether the population had experienced one or
more demographic threats. Populations were categorized
as “demographically challenged” if authors identified one
or more of these risk factors as affecting the population.
When no such demographic threats were reported, populations were considered “healthy.”
We evaluated genetic diversity at the population level
and then summarized the results by species to avoid a
lack of statistical independence among populations of
the same species. When studies included both populations that had experienced a demographic threat and
those that had not, however, average heterozygosities
were recorded separately for those population categories.
Species mean heterozygosities were transformed to the
arc-sine square root for statistical analyses (Zar 1999). We
report means ± SE.
We evaluated current patterns of heterozygosity across
body masses and taxonomic groups. Average body masses
were obtained from the following sources: the CRC Handbook of Mammalian Body Masses (Silva & Downing
1995), the American Society of Mammalogists (19692004) Mammalian Species Accounts, The Mammalian
Radiations (Eisenberg 1981), species action plans, or
similar suitable sources. We used average female body
mass for those species exhibiting marked sexual size dimorphism. Body masses were log transformed and linear regression was used to test the hypothesis that genetic diversity varied with mammalian body mass (Zar
1999). We contrasted heterozygosity levels between placental (eutherian) and marsupial (metatherian) mammals
with a t test. A nested analysis of variance (ANOVA) was
used to examine partitioning of variation in heterozygosity among orders and among families within orders (Oli
& Dobson 2003). Only populations that had not experienced a demographic threat were used in analyses of
background patterns of genetic diversity.
We tested the hypothesis that diversity levels differed
between populations that had and had not experienced
a demographic threat by contrasting current levels in
populations in both categories. We used a t test to contrast healthy and demographically challenged populations
across species and a paired t test for a contrast within
species. Because ascertainment bias may influence crossspecies comparisons, we included ascertainment as a
covariate in analyses of heterozygosity differences between healthy and threatened populations. Only studies
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Volume 19, No. 4, August 2005
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Mammalian Genetic Diversity
Figure 1. Average heterozygosity (transformed to the
arc-sine square root) of all mammal species examined
relative to body mass (r 2 = 0.003, p = 0.637, n = 82).
Only healthy populations were included in this
analysis.
that reported primers as either species specific or cross
species for all loci were included in analyses of ascertainment bias. Lastly, we used a Wilcoxon paired-sample test
(Zar 1999) to evaluate ascertainment within studies that
used both species-designed and transferred primers.
Results
Analyses of genetic diversity in healthy populations of
mammals revealed few consistent background patterns.
Heterozygosity and body mass were not related. Linear
regressions were nonsignificant for all mammals (Fig. 1)
and for placentals (n = 71) and marsupials (n = 11) when
analyzed independently (r 2 = 0.001, p = 0.802 and r2 =
0.034, p = 0.588, respectively). Levels of genetic diversity differed among higher order mammalian taxa in the
studies we reviewed. Marsupials exhibited significantly
higher levels of heterozygosity (mean = 0.765 ± 0.02, n =
11) than placental mammals (mean = 0.677 ± 0.01, n =
74; t = −3.193, p = 0.006). Although differences were
apparent at the infraclass level, microsatellite heterozygosity was not partitioned by lineage among orders of
placental mammals (nested ANOVA: F = 0.96, p = 0.440,
df = 4). Within orders, diversity did differ among families in this sample (F = 3.43, p = 0.006, df = 7; Fig. 2).
The nested ANOVA included only families represented
by ≥3 species, however, which comprised only 12 out
of 34 families in our total data set (available from authors upon request). Therefore, evidence for systematic
differences in heterozygosity based on phylogeny is limited. However, because heterozygosities differed between
placental and marsupial mammals, we examined genetic
diversity relative to demographic history independently
for each group. These comparisons included only healthy
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Garner et al.
populations and therefore do not reflect heterozygosity
levels in populations that had experienced demographic
threats.
Our analyses demonstrated a consistent loss of genetic
diversity in populations that had experienced a demographic threat. Demographically challenged populations
of mammals exhibited lower heterozygosity than healthy
populations (Fig. 3). Mean heterozygosity was significantly lower in populations that had experienced a demographic threat for both marsupials (healthy = 0.765
± 0.024, n = 11; demographically challenged = 0.597 ±
0.051, n = 11) and placentals (healthy = 0.677 ± 0.012, n
= 74; demographically challenged = 0.502 ± 0.027, n =
28). Reduction in mean heterozygosity was similar in both
taxa (26% and 22%, respectively). For 16 species, data
were available for both demographically challenged and
healthy populations, and as in the broader comparison,
populations that had experienced a demographic threat
had a significantly reduced (0.19 ± 0.37, 27%) mean heterozygosity in the paired data set (healthy mean = 0.715
+ 0.24, demographically challenged mean = 0.525 +
0.04; paired t = 5.088, p = 0.000, n = 16). These results indicate a strong association of demographic threats
and lower genetic variability across a wide range of mammalian taxa.
Ascertainment bias also significantly and consistently
affected levels of heterozygosity in both demographically
challenged and healthy populations. Both ascertainment
(F = 6.995, p = 0.010, n = 93) and population demographic history (F = 31.395, p = 0.000, n = 93) significantly affected mean heterozygosity in a contrast that
included both marsupial and placental mammals. The latter result represents a conservative test because a greater
percentage of marsupial populations, which exhibited
higher heterozygosity than placental mammals, was included in the demographically challenged category. Average heterozygosity was reduced by 0.07 when crossspecies primer application occurred, which represented
a reduction of 13% and 10% for demographically challenged and healthy populations, respectively.
A more rigorous test of ascertainment bias was a comparison of genetic diversity within studies that used
primers designed for the study species and primers transferred from other species. We identified those mammalian
studies that used at least three primers from each category
(Table 1). Estimates of heterozygosity calculated using the
transferred primers were significantly lower ( p < 0.05)
than values obtained using the species-specific primers.
Heterozygosity was reduced by an average of 0.06 in this
comparison within species, which is comparable to the
reduction observed in the broader comparison across
species. Additionally, the mean number of alleles per locus was significantly lower ( p ≤ 0.02) at microsatellite
loci identified using transferred primers. Although this
measure was more sensitive to small sample sizes, the
values from transferred primers were lower in all cases.
Garner et al.
Mammalian Genetic Diversity
1219
Figure 2. Average heterozygosity
(± SE) across mammalian
families. Only families
represented by at least three
species and healthy populations
are included.
Discussion
Mammals are a familiar and well-studied taxon, yet an understanding of genetic patterns across the class is limited.
Studies of mammalian allozyme diversity have produced
conflicting results. Our results provide a first, coarse
quantification of background patterns of genetic diversity
Figure 3. Genetic diversity in mammal populations
relative to population history of demographic threat
(reduction in population size or range, bottleneck, or
isolation from conspecifics). Error bars represent 95%
confidence intervals.
and its loss across mammals assessed with microsatellite
markers.
Our analysis of populations from 82 mammalian species
ranging in size from shrews to whales did not support
the hypothesis that larger bodied mammals should exhibit lower levels of genetic diversity. These results, based
on microsatellite diversity, differ from some allozyme
studies reporting lower heterozygosity in large mammals
(Selander & Kaufman 1973; Wooten & Smith 1985) but
concur with other research indicating little variation in
allozyme heterozygosity across mammalian taxa (Baccus et al. 1983; Makarieva 2001). In the latter result,
Makarieva’s (2001) calculations were corrected for percent polymorphic loci, a correction that renders allozyme
data more analogous to data in microsatellite studies,
which generally do not report nonpolymorphic loci. Although both marker types may reveal similar patterns, microsatellites exhibit much greater variability (average heterozygosity of 0.69 across mammals as opposed to 0.05
for allozymes), allowing genetic variation to be quantified on a finer scale. We suggest that mammalian body
size does not contribute to patterns of genetic diversity
across species.
Likewise, we did not find a consistent trend in genetic
diversity in healthy populations across mammalian taxa.
We observed differences in heterozygosity at the highest taxonomic level, between populations of marsupial
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Mammalian Genetic Diversity
Garner et al.
Table 1. Microsatellite data from studies that used both primers designed for the study species and primers transferred from other species.
Primers from study species
Species
Odobenus rosmarus
Lasiorhinus krefftii
Lasiorhinus latifrons
Phoca vitulina
Ctenomys haigi
Ursus arctos
Spermophilus brunneus
He
no. alleles
no. loci
He
no. alleles
Reference
6
12
11
3
7
8
4
0.758
0.418
0.716
0.516
0.708
0.693
0.551
7.00
2.67
6.27
7.02
8.43
6.03
4.12
3
8
16
4
8
11
4
0.515
0.486
0.691
0.459
0.692
0.638
0.449
4.25
2.50
4.94
3.63
6.63
5.52
3.33
Anderson et al. 1998
Behergaray et al. 2000
Behergaray et al. 2000
Goodman 1998
Lacey 2001
Waits et al. 2000
Garner 2004
and placental mammals. However, there was no significant pattern in diversity among orders of placental mammals, and analyses at the family level most likely were
influenced by small sample sizes. Additional research is
needed to provide a rigorous test of phylogenetic patterns.
Nonetheless, there was a pervasive and consistent reduction in genetic diversity in populations that had experienced a demographic threat across a broad array of mammals, both rare and common. Populations that had experienced one or more demographic challenges exhibited
>20% lower heterozygosity. Frankham et al. (2002) notes
that endangered species have lower genetic diversity than
nonendangered ones. Our analyses extend this outcome
to the population level, suggesting that even some unprotected species are currently losing genetic diversity
in demographically threatened populations. Loss of genetic diversity increases vulnerability to environmental,
demographic, and stochastic variation and consequently
increases probability of extinction (Mills & Smouse 1994;
Lacy 1997; Frankham et al. 2002). Therefore, even populations of common species can enter the “extinction
vortex” (Gilpin & Soulé 1986). Our results suggest that
populations of many mammalian species may be moving
in that direction.
In our analyses, demographically challenged populations exhibited reduced genetic diversity even after accounting for ascertainment bias. Studies that used primers
developed for other species reported lower levels of heterozygosity, and within studies transferred primers also
resulted in significantly lower diversity values. These results suggest that further research is needed to quantify
the full effect of ascertainment on assessments of genetic
diversity. Although microsatellite primers are commonly
transferred across taxa (e.g., Menotti-Raymond & O’Brien
1995; Engel et al. 1996; Webster et al. 2002), caution
should be applied in making comparisons and drawing
conclusions across studies unless ascertainment bias has
been considered.
Much conservation effort focuses at the species level.
Extinction rates for populations, however, are estimated
to be three to eight times higher than for species (Hughes
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Volume 19, No. 4, August 2005
Primers from other species
no. loci
et al. 1997). Therefore, substantial losses in genetic diversity most likely occur at the population level before
conservation action at the species level. The erosion of
mammalian genetic diversity we demonstrate here suggests that conservation policy may need to focus below
the species level to stem further losses. Although distinct
population segments can be listed as threatened or endangered under the U.S. Endangered Species Act, species
are disproportionately listed (Tear et al. 1993). By the
time a species (or even a distinct population segment
of a species) receives conservation status, it may have already lost a substantial portion of its genetic wealth. Comprehensive strategies aimed at capturing the full range
of remaining biodiversity should include efforts to conserve genetic diversity within populations, which may be
missed in species-based conservation approaches.
Acknowledgments
Funding for A. Garner was provided by the Berklund Foundation and the University of Idaho. We thank J. M. Scott,
L. Waits, C. Miller, D. Roon, J. Sullivan, F. S. Dobson, and
an anonymous reviewer for comments, suggestions, and
insights that improved the manuscript.
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Conservation Biology
Volume 19, No. 4, August 2005