Advancing Sustainable Materials Management: Facts and Figures
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Accredited Sur. Rosen v. County of L. However, the phylogeographic patterns between eastern, western, and island Urocyon populations had not been determined. Mitochondrial DNA is a powerful marker for dating mammalian divergences and mitogenomes and has been used to examine both phylogeographic and evolutionary relationships in wild and domesticated animals, including canids [ 28 — 32 ].
Here, we present the first application of high throughput sequencing HTS of whole mitochondrial genomes mitogenomes to evaluate the phylogeographic patterns of differentiation between island and mainland gray fox populations. Our goal is to reconstruct the evolutionary history of island and gray foxes and to unravel their patterns of colonization into the Channel Islands. We address the following questions: 1 When did foxes reach the Channel Islands? We sequenced complete mitogenomes from modern — island foxes from the six islands in their current range and 25 gray foxes — from across California Fig.
De Novo assembly revealed a 16, bp gray fox mitogenome with a mean read depth of x. However, a short fragment bp of the D-loop was excluded from all subsequent analyses due to problems with assembly and mapping of repetitive regions, leaving an alignment of 16, bp for all foxes. Mean read depth for all samples ranged from 33 to x std. The mitogenome sequences revealed a total of 35 haplotypes with 14 found exclusively on the islands and 21 found only in mainland California. Haplotype and nucleotide diversity in the island populations was markedly lower than in the mainland populations, with only one to five haplotypes per island.
The northern islands had nine closely related haplotypes while the southern islands had five haplotypes that were more distant from each other Fig.
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All of the islands had a least one private haplotype, but 19 of 41 Santa Catalina foxes southern island shared a haplotype with Santa Cruz foxes northern island. No other islands shared a haplotype, although San Clemente and San Nicolas each had two haplotypes that were separated by a single base pair. Independent analyses of two of the most widely used mtDNA genes in mammalian phylogeography, cytochrome b and D-loop, recovered only 15 and 20 haplotypes, respectively, instead of the 35 haplotypes recovered by sequencing whole mitogenomes S2 Table.
These two genes represent a reduced portion of the genetic variation of island and mainland foxes as demonstrated by single-gene median joining networks S1 Fig. Across the entire mitogenome, island foxes showed a three-fold reduction in the proportion of variable sites compared to mainland gray foxes S2 Table. A Median joining network using the variable sites of the mitochondrial genome was generated in the program Network v.
The size of the circles and branch lengths are proportional to number of individuals represented and the number mutations between haplotypes red , respectively. Hash marks indicate shortened branches. Santa Catalina and Santa Cruz are the only islands that share a haplotype, which is more closely related to the northern island haplotypes than the southern. To evaluate the patterns of selective pressures acting on mainland and island fox mitogenomes, we estimated the proportion of nonsynonymous dN and synonymous variable dS sites throughout all of the protein-coding genes Table 2.
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Archaeological and paleontological research has identified more than fox bones from more than 35 different archaeological and subfossil sites across the archipelago. Many of the bones have relatively secure associated radiocarbon ages; all of which are more recent than cal BP [ 18 , 19 , 21 ]. Morphological analysis of these ancient bone samples indicate the characteristic island fox morphology, even in the oldest sites [ 19 ].
To investigate the antiquity of foxes on the Channel Islands and improve radiocarbon chronologies, we obtained three new AMS radiocarbon dates of island fox bones from the potentially earliest archaeological contexts to complement previously published AMS dates. This yielded a total of nine directly radiocarbon dated ancient fox bones S3 Table. We found no fossil or archaeological evidence of foxes on any of the Channel Islands prior to cal BP.
Our AMS dated samples show phenotypic characteristics of island foxes i. Fox bones with the characteristic gray fox morphology have been recovered from relatively few archaeological sites on the coastal mainland; none have been recovered on the Channel Islands. Similarly, no small fox has been identified in mainland assemblages. This tree yielded the same topology as a maximum likelihood analysis with Vulpes and Canis outgroups; both trees had strong support S2 Fig.
Advancing Sustainable Materials Management: Facts and Figures
Our phylogenetic analysis Fig. However, gray foxes from southern and northern California did not show a strong pattern of contemporary phylogeographic structure, and their haplotypes did not form reciprocally monophyletic clades. Haplotypes in clade A included all individuals sampled in southern California, plus some haplotypes from northern California.
Remarkably, island fox haplotypes formed a monophyletic clade nested within clade B, rather than with foxes from southern California, closest to the Channel Islands.
Note that central California is our weakest sampling area. Future studies should focus on obtaining samples in this region. Northern California purple and southern California gray foxes show patterns of climate-induced expansion. Local temperature curves were not used due to the geographic distance sampled and the short time scale of local curves. A broad scale analysis of the evolutionary relationships of Urocyon lineages should be conducted because in this study, we found that eastern and western gray fox populations are more deeply diverged than the two currently recognized species of California Urocyon S2 Fig.
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Furthermore, the island fox mitogenomic diversity Fig. Adaptive divergence between island and mainland populations is likely and nuclear data will be important for re-examining species and sub-specific designations. We propose the following hypothesis for the phylogeographic pattern observed in clade A California mainland gray foxes: During the late Pleistocene, approximately 23, years ago Fig. Glacial climatic fluctuations caused habitat changes, including the appearance of continental ice sheets as far south as Washington State [ 37 ], that may have caused range shifts in locally adapted gray fox populations, with foxes with clade B haplotypes existing as far south as southern California.
The current northern range extension of gray foxes is well into northern Oregon. However, the climate-induced shifts in habitat that occurred during the late Pleistocene, may have influenced a southward shift in the distributional range of gray foxes. As the climate warmed during the Holocene, and suitable habitat expanded northward, gray fox population ranges shifted further north resulting in foxes with clade A haplotypes distributed as far north as Shasta County in northern California Fig. Niche modeling with finer-scaled sampling and further genetic analysis is needed to test our hypothesis.
Interestingly, a similar climatic-induced, phylogeographic pattern was found in eastern gray foxes [ 27 ]. The historic expansion of gray foxes into northeastern US during the Medieval Climate Anomaly may have coincided with the expansion of eastern deciduous forests [ 27 ]. Island foxes form a monophyletic group within the northern California gray fox clade Clade B; Fig. Santa Catalina and Santa Cruz foxes share a haplotype Fig. This scenario is supported by similarities between these islands in morphological and mtDNA restriction hybridization data collected before and the later fox population bottlenecks [ 15 , 20 ].
Santa Catalina was a center for trade between Native Americans on the mainland and the southern and northern Channel Islands, with evidence for exchange of a variety of goods including soapstone artifacts from Santa Catalina quarries [ 20 , 38 ]. Sample size does not account for this pattern as mitogenome sample sizes were larger on all islands except Santa Rosa and San Nicolas. San Nicolas island foxes were found to be monomorphic at 18 microsatellite loci but showed higher heterozygosity in MHC loci [ 17 ]. We identified two pairs of closely related haplotypes on each of the two most remote islands in the archipelago San Nicolas and San Clemente , which indicates in situ evolution of island fox genetic variation.
Furthermore, the fox populations on San Nicolas and San Clemente islands did not undergo as severe population crashes as the other island fox populations experienced. This might explain the presence of additional haplotypes, especially in comparison to the population crashes and the potential loss of genetic diversity on San Miguel and Santa Catalina.