Transcript Impacts of beach nourishment on loggerhead and green

Evolution of the African ground squirrel genus Xerus:
Phylogenetic and phylogeographic patterns reflect the influence of climate change
Matthew D. Herron, Christopher L. Parkinson and Jane M. Waterman
Department of Biology, University of Central Florida
Spermophilopsis leptodactylus
Abstract: We used Bayesian and maximum parsimony
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phylogenetic methods and nested clade analysis to infer
relationships among African ground squirrels (Xerus) using
mitochondrial cytochrome b sequences. We inferred
relationships among the four species of Xerus, evaluated the
specific distinctness of Cape (X. inauris) and mountain (X.
princeps) ground squirrels, and tested hypotheses for historical
patterns of gene flow within X. inauris. The inferred phylogeny
supports the existence of an “arid corridor” from the Horn of
Africa to the Cape region until at least the Early Pleistocene. Our
analyses suggest that X. inauris and X. princeps represent
distinct monophyletic lineages, and thus appear to be valid taxa.
Phylogenetic and phylogeographic patterns suggest distinct
effects of climate change on population differentiation and
speciation within Xerus.
X. rutilus 65
X. rutilus 66
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Ameib Xp 49
Hobitere Xp 59
Clade I
Ameib Xp 60
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Losberg Xp 22
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Losberg Xp 24
Clade II
57 Nazerus Xp 28
84 Nazerus Xp 39
Kalkrand Xp 68
Fish River Canyon Xp 69
Berghoff Xi 55
Berghoff Xi 57
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Namib Xi 32
99
Namib Xi 34
Clade I
Namib Xi 35
Namib Xi 44
Namib Xi 42
Namib Xi 45
Ameib Xi 47
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SA Lombard Xi 83
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SA Lombard Xi 82
100 SA Lombard Xi 89
Clade II
96 Vrede Xi 115
Benfontein Xi 110
Benfontein Xi 111
Gross Aub Xi 75
99
Kingsrest Xi 78
91
SA Lombard Xi 84
Ameib Xi 48
Ameib Xi 50
Ameib Xi 51
100
Kranzberg
Xi 61
97
Groot Hakos Xi 90
Christirina Xi 93
Christirina Xi 94
Van Zylsius Xi 80
Van Zylsius Xi 81
Christirina Xi 07
Christirina Xi 14
Christirina Xi 09
Christirina Xi 91
Eschenhof Xi 85
Eschenhof Xi 86
Eschenhof Xi 87
Eschenhof Xi 88
Weldevrede Xi 31
Weldevrede Xi 29
Weldevrede Xi 23
Clade III
Weldevrede Xi 26
Weldevrede Xi 33
Weldevrede Xi 37
Weldevrede Xi 38
Weldevrede Xi 40
Oorwinning Xi 25
Oorwinning Xi 36
Christirina Xi 17
Christirina Xi 19
Christirina Xi 08
Christirina Xi 06
Christirina Xi 10
Christirina Xi 12
Christirina Xi 18
Christirina Xi 21
Christirina Xi 27
Christirina Xi 92
Gochas Xi 72
Gochas Xi 73
Kingsrest Xi 77
Osterodenord Xi 70
Osterodenord Xi 71
Gross Aub Xi 74
Kingsrest Xi 76
Namib Rand Xi 95
Namib Rand Xi 96
Namib Rand Xi 97
Namib Rand Xi 98
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Introduction: Africa has undergone several major episodes of
climate change since the Pliocene, which likely caused shifts in
vegetation. Several authors have hypothesized that an “arid
corridor” stretched from the Horn of Africa to the Cape of Good
Hope during drier periods, providing a route by which xeric plants
and animals dispersed from central to southern Africa. This
hypothesis is supported by disjunct distributions of several aridadapted plant taxa found in both southern and eastern Africa.
The ground squirrel tribe Xerini (Sciuridae) is an example
of an arid-adapted animal taxon with a disjunct distribution in
Africa. Two of the three extant genera in this tribe are endemic to
Africa. The Barbary ground squirrel, Atlantoxerus getulus, is
restricted to the extreme northwest of Africa, while the genus
Xerus is broadly distributed across the arid and semiarid zones
of sub-Saharan and southwest Africa. The third member, the
long-clawed ground squirrel (Spermophilopsis leptodactylus),
occupies a range east of the Caspian Sea in central Asia.
The four species making up the genus Xerus occupy two
disjunct ranges separated by nearly 2000 km (Fig. 1). With the
exception of X. erythropus, which occupies a variety of habitats,
Xerus is restricted to arid semi-desert and savannah habitats.
The striped ground squirrel (X. erythropus) and the unstriped
ground squirrel (X. rutilus) occupy overlapping ranges in subSaharan Africa, while the Cape ground squirrel (X. inauris) and
the mountain ground squirrel (X. princeps) occupy overlapping
ranges in the southern Africa. Pleistocene changes in
precipitation patterns are likely to have fragmented arid habitats
in southern Africa (Matthee & Flemming 2002), thus present
patterns of genetic structure in arid-adapted taxa may have been
significantly impacted by past isolation of populations in xeric
refugia.
Xerus inauris and X. princeps are almost morphologically
indistinguishable and occur sympatrically in portions of their
respective ranges. Both are terrestrial, semi-fossorial and diurnal
(Dorst & Dandelot 1970). In spite of their morphological and
ecological similarities, X. inauris and X. princeps have strikingly
different social behaviors; X. inauris forms large bands, whereas
X. princeps is mainly solitary (Herzig-Straschil & Herzig 1989;
Waterman 1995). Female X. inauris live in highly social kin
clusters of up to three adult females and subadult offspring
(Waterman 1995; Waterman 1997). Males form social groups
composed of unrelated individuals; their range overlaps the
ranges of several female social groups (Waterman 1995;
Waterman 1997). Both males and females forage as groups and
share sleeping burrows (Waterman 1995).
Little is known regarding the phylogeny of the Xerini, and
several studies have presented conflicting hypotheses for their
phylogenetic position within the Sciuridae. Here, we (1) infer
phylogenetic hypotheses for the evolutionary relationships
among the four currently recognized species of the genus Xerus,
(2) investigate the historical biogeographic patterns leading to
the current distributions of Xerus species, and (3) investigate the
roles of gene flow and climate change in the phylogeographic
history of X. inauris.
X. erythropus 67
X. erythropus 113
X. erythropus 114
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Figure 1.
Map of Africa showing ranges of Atlantoxerus getulus
(vertical stripes), Xerus erythropus (dots), X. inauris (light gray), X.
princeps (diagonal stripes) and X. rutilus (dark gray). Inset: southern
Africa with ranges and sampling localities for Xerus inauris (clade I:
gray circles; clade II: white circles; clade III: black circles; see text) and
X. princeps (squares).
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Figure 1.
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Map of Africa showing ranges of Atlantoxerus getulus
(vertical stripes), Xerus erythropus (dots), X. inauris (light gray), X.
princeps (diagonal stripes) and X. rutilus (dark gray). Inset: southern
Africa with ranges and sampling localities for Xerus inauris (clade I:
gray circles; clade II: white circles; clade III: black circles; see text) and
X. princeps (squares).
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• MP and MCMC resolved the same major clades.
• Xerus erythropus is basal to the remaining Xerus.
• The sister group to (X. inauris + X. princeps) is X. rutilus.
• Xerus inauris is sister to X. princeps, and each is monophyletic.
• Within X. princeps, a northern (Clade I) and a southern (Clade II) clade were
resolved.
• Three major clades were resolved within X. inauris: clade I, restricted to westcentral Namibia; clade II, restricted to South Africa east and south of the
Kalahari, and clade III, overlapping the distributions of clades I and II.
• Nested clade analysis of X. inauris:
• All haplotypes were included within three four-step clades (4-1 through 4-3 in
Fig. 3), which correspond to the three major clades recovered in the MP and
MCMC analyses (Fig. 2).
•Restricted gene flow (RGF) with isolation by distance (IBD) was evident in two
high level clades, including the total cladogram.
• Two third-level clades (3-1 and 3-3) exhibited IBD or long distance dispersal
(LDD), and one third level clade (3-2) showed past habitat fragmentation.
Conclusions:
• Xerus phylogeny is consistent with the former existence of a hypothesized “arid
corridor” running from the Horn of Africa to the Cape of Good Hope. Fossils
identified as Xerus cf. inauris, dated from 1.75 MYA, in the Olduvai Gorge of
Tanzania (Fernandez-Jalvo et al. 1998) suggest that X. inauris may have originated
in eastern Africa near the current range of X. rutilus.
• Recognition of X. princeps and X. inauris as distinct species is warranted.
Restriction of X. princeps to the western escarpment underscores the importance
of adding all or part of this region to Namibia’s network of protected lands.
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Results:
• Phylogenetic analyses:
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Map of Africa showing ranges of Atlantoxerus getulus
(vertical stripes), Xerus erythropus (dots), X. inauris (light gray), X.
princeps (diagonal stripes) and X. rutilus (dark gray). Inset: southern
Africa with ranges and sampling localities for Xerus inauris (clade I:
gray circles; clade II: white circles; clade III: black circles; see text) and
X. princeps (squares).
Methods: We extracted total DNA using proteinase K digestion followed
by phenol/chloroform/isoamyl alcohol organic separation methods. We
PCR-amplified the cyt b gene using 45 cycles of denaturation at 94°C for 1
min, annealing at 45-60°C for 1 min, and extension at 72°C for 2 min. PCR
products were excised from agarose gels and purified using the MinElute™
Gel Extraction kit (Qiagen). All sequencing reactions were run using the
CEQ Dye Terminator Cycle Sequencing Quick Start Kit (Beckman Coulter),
electrophoresed on a Beckman CEQ8000 automated sequencer,
according to the manufacturer’s protocols.
We edited raw sequence chromatographs in Sequencher 4.1.2
(Gene Codes Corp.) and aligned sequences manually in GeneDoc 2.6.002
(Nicholas & Nicholas 1997). We estimated phylogenetic relationships
using both Bayesian Metropolis-coupled Markov Chain Monte Carlo
(MCMC) and maximum parsimony (MP) methods. A cyt-b sequence from
Spermophilopsis leptodactylus was the outgroup for all analyses. All
MCMC phylogenetic reconstructions were conducted in MrBayes Version
3.0b4 (Ronquist & Huelsenbeck 2003), with nodal support evaluated by
posterior probabilities. We conducted equally-weighted MP searches in
PAUP* v4.0b10 (Swofford 2002) and assessed nodal support with
nonparametric bootstrapping. We constructed statistical parsimony
networks for X. inauris using a 95% confidence limit in TCS Version 1.13
(Clement et al. 2000). We nested the resulting haplotype network following
the procedures outlined in Templeton et al. (1987), Templeton & Sing
(1993) and Crandall (1996). We performed nested contingency analysis
and nested geographical distance analysis using GeoDis Version 2.0
(Posada et al. 2000) and interpreted the results using the revised
inference key (http://inbio.byu.edu/Faculty/kac/crandall_lab/geodis.htm).
• Gene flow among populations of X. inauris was restricted due to isolation by
distance early in the species’ evolutionary history. Suitable habitat for X. inauris
was widespread and essentially uninterrupted throughout the SWA early in the
species’ evolution, as it is today.
• A more recent restriction of gene flow resulted from habitat fragmentation in
southern Africa, probably due to intermittently wetter conditions. The return of drier
conditions allowed isolated populations of X. inauris to expand, eventually coming
into secondary contact. This inferred secondary contact of X. inauris clades is
observed in western Namibia and northern South Africa.
Acknowledgements: We thank Suzanne B. McLaren of the Division of Mammals, Carnegie
Museum of Natural History, for providing two samples of Xerus rutilus; Dr. Mary Denver of the
Baltimore Zoo for providing a sample of X. erythropus; and Dr. Eileen Lacey for providing samples of
X. erythropus and X. inauris. Additional thanks go to Beryl Wilson of the McGregor Museum, Kimberly,
South Africa and Alexandra Jo Newman for help collecting samples. We also thank Todd Castoe, John
Fauth, James Roth and Franklin Snelson for their suggestions and comments on various drafts of the
manuscript. This work was supported, in part, by a Graduate Thesis Grant from the University of
Central Florida Department of Biology and by NSF grant #0130600.