The population genetics of nonmigratory Allen’s Hummingbird (Selasphorus sasin sedentarius) following a recent mainland colonization

Allen''s Hummingbird comprises two subspecies, one migratory (Selasphorus sasin sasin) and one nonmigratory (S. s. sedentarius). The nonmigratory subspecies, previously endemic to the California Channel Islands, apparently colonized the California mainland on the Palos Verdes Peninsula some time before 1970 and now breeds throughout coastal southern California. We sequenced and compared populations of mainland nonmigratory Allen''s Hummingbird to Channel Island populations from Santa Catalina, San Clemente, and Santa Cruz Island. We found no evidence of founder effects on the mainland population. Values of nucleotide diversity on the mainland were higher than on the Channel Islands. There were low levels of divergence between the Channel Islands and the mainland, and Santa Cruz Island was the most genetically distinct. Ecological niche models showed that rainfall and temperature variables on the Channel Islands are similar in the Los Angeles basin and predicted continued expansion of nonmigratory Allen''s Hummingbird north along the coast and inland. We also reviewed previous genetic studies of vertebrate species found on the Channel Islands and mainland and showed that broad conclusions regarding island–mainland patterns remain elusive. Challenges include the idiosyncratic nature of colonization itself as well as the lack of a comprehensive approach that incorporates similar markers and sampling strategies across taxa, which, within the context of a comparative study of island–mainland relationships, may lead to inconsistent results.     

Dictyota cyanoloma (Dictyotales,Phaeophyceae), a Newly Introduced Brown Algal Species in California

Here, we report for the first time the presence of Dictyota cyanoloma in southern California. Dictyota cyanoloma is conspicuous in harbors and bays by its distinctive bright blue‐iridescent margins. This species was originally described from Europe, but subsequent studies have revealed that it represented an introduction from Australia. The current distribution of D. cyanoloma comprises southern Australia and the North East Atlantic, including the Mediterranean Sea and the Macaronesian islands. The presence of D. cyanoloma in southern California is supported by molecular cox1 and psbA gene sequences. A reconstruction of the invasive history based on nine polymorphic microsatellite markers reveals a close affinity of the Californian specimens with European populations. Dictyota cyanoloma in the United States appears to be (so far) restricted to the Californian coast from San Diego Bay in the south to Santa Catalina Island and Long Beach Harbor in the north. A correlative species distribution model suggests gradually declining habitat suitability north of the Southern Californian Bight and high suitability in Baja California, including the Gulf of California. Finally, its widespread abundance in bays and harbors suggests shipping is a likely transport mechanism.     

Host islands within the California Northern Channel Islands create fine-scale genetic structure in two sympatric species of the symbiotic ectomycorrhizal fungus Rhizopogon

We have examined fine-scale genetic structure of the symbiotic ectomycorrhizal fungi Rhizopogon occidentalis and R. vulgaris on two of the California Channel Islands using five and six microsatellite loci, respectively. Both Rhizopogon species are sympatric on Santa Cruz and Santa Rosa Islands and are ectomycorrhizal with bishop pine (Pinus muricata) on both islands or Santa Rosa Island Torrey pine (P. torreyana ssp. insularis) on Santa Rosa. The combination of disjunct pine host distributions and geographic barriers within and among the islands have created highly structured Rhizopogon populations over very short distances (8.5 km on Santa Cruz Island; F(ST) = 0.258, F(ST) = 0.056, R. occidentalis and R. vulgaris, respectively). Both species show similar patterns of genetic differentiation as a result of limited dispersal between host populations as revealed by a significant isolation by distance relationship (r = 0.69, P < 0.04; r = 0.93, P < 0.001, R. occidentalis and R. vulgaris, respectively) and Bayesian clustering analyses, and is most likely a function of the small foraging range of the few mammals that disperse Rhizopogon on these islands and the enormous spore bank characteristic of Rhizopogon species.     

Genetic analysis of the endemic island loggerhead shrike, <Emphasis Type="Italic">Lanius ludovicianus anthonyi</Emphasis>

Based on limited research, the island loggerhead shrike, Lanius ludovicianus anthonyi has been considered a distinct subspecies endemic to the northern California Channel Islands. We used mtDNA control region sequences and microsatellite genotyping to compare loggerhead shrikes from the southern California mainland (L. l. gambeli), San Clemente Island (L. l. mearnsi), and the northern islands (L. l. anthonyi). Habitats on the islands are recovering due to the removal of non-native ungulates on the islands, but may be transitioning to habitats less supportive of loggerhead shrikes, so this evaluation comes at a critical time. We utilized 96 museum specimens that were collected over a century to evaluate both spatial and temporal genetic patterns. Analysis of multilocus microsatellite genotypes indicated that historical specimens of loggerhead shrikes (collected between 1897 and 1986) from the two northern islands of Santa Rosa and Santa Cruz are genetically distinct from adjacent mainland and island shrikes. Birds from Santa Catalina Island showed mixed ancestry and did not cluster with the northern island birds. Historical specimens of L. l. mearnsi from San Clemente Island also showed mixed ancestry. Our study provides evidence that a genetically distinct form of loggerhead shrikes, L. l. anthonyi, occurred on the islands of Santa Rosa and Santa Cruz.     

Porotic hyperostosis in a marine-dependent California Indian population

A maize-based iron- and protein-deficient diet is commonly cited as the most important cause of porotic hyperostosis among American Indian agriculturalists. An alternative to this maize dependence hypothesis is suggested by the analysis of 432 crania from the nonagricultural, fish-dependent population of the Channel Island area of southern California. Cribra orbitalia, a form of porotic hyperostosis associated with iron deficiency anemia, is just as common among these fisherpeople, whose diet was rich in iron and essential amino acids, as it is among maize-dependent agriculturalists. Northern Channel Island crania have much more cribra orbitalia than those from the California mainland. The highest incidence is on San Miguel, a small geographically isolated island with a shortage of fresh water and terrestrial resources. The Indians who lived on Santa Cruz, the largest of the northern Channel Islands with the greatest diversity of terrestrial plants and animals, have less cribra orbitalia than those who lived on Santa Rosa or San Miguel Island. This geographical distribution appears to be explained by island-mainland and interisland differences in water contamination, exposure to fish-borne parasites, and nutritional adequacy of the diet. The prevalence of porotic hyperostosis in a population with a heavy dietary dependence on marine resources shows that among prehistoric American Indians, this condition is not always associated with an iron- and protein-deficient diet of cultigens. It seems likely that high nutrient losses associated with diarrheal disease are often more significant in the etiology of porotic hyperostosis than a low dietary intake of essential nutrients.     

Genetic Divergence of an Avian Endemic on the Californian Channel Islands

The Californian Channel Islands are near–shore islands with high levels of endemism, but extensive habitat loss has contributed to the decline or extinction of several endemic taxa. A key parameter for understanding patterns of endemism and demography in island populations is the magnitude of inter–island dispersal. This paper estimates the extent of migration and genetic differentiation in three extant and two extinct populations of Channel Island song sparrows (Melospiza melodia graminea). Inter–island differentiation was substantial (G''''_ST: 0.14–0.37), with San Miguel Island having the highest genetic divergence and lowest migration rates. Santa Rosa and Santa Cruz Island populations were less diverged with higher migration rates. Genetic signals of past population declines were detected in all of the extant populations. The Channel Island populations were significantly diverged from mainland populations of M. m. heermanni (G''''_ST: 0.30–0.64). Ten mtDNA haplotypes were recovered across the extant and extinct Channel Island population samples. Two of the ten haplotypes were shared between the Northern and Southern Channel Islands, with one of these haplotypes being detected on the Californian mainland. Our results suggest that there is little contemporary migration between islands, consistent with early explanations of avian biogeography in the Channel Islands, and that song sparrow populations on the northern Channel Islands are demographically independent.     

Typological thinking and the conservation of subspecies: the case of the San Clemente Island loggerhead shrike

Abstract.  Hybridization with closely related taxa poses a significant threat to endangered subspecies (e.g. outbreeding depression, inbreeding) and confounds efforts to manage and conserve these taxa through a loss of taxonomic identity, in part because of the practical necessity of defining subspecies in a typological manner. We examined nine morphological characters in 167 post-juvenile museum specimens to determine if loggerhead shrikes Lanius ludovicianus Linnaeus 1766 on San Clemente Island (off the coast of California) remain diagnosable as L. l. mearnsi Ridgway (1903); an island endemic listed as endangered by the United States Fish and Wildlife Service. Four recent shrike specimens from the island were compared to historical specimens using a bivariate scatter plot and a discriminant function (the latter was used to classify recent specimens post hoc). The few recent specimens were not diagnosable as L. l. mearnsi , but instead appear to be intergrades between L. l. mearnsi and L. l. anthonyi Mearns 1898 (the subspecies endemic to Santa Cruz, Santa Catalina, Santa Rosa and Anacapa islands), and are perhaps closer to pure anthonyi . Our data and the species' natural history and distribution suggest that shrikes currently on San Clemente Island are the result of genetic 'swamping' of mearnsi by anthonyi . Under a necessarily typological definition of a subspecies, it is evident that mearnsi is probably no longer diagnosable. However, we conclude that protection of the entire Channel Islands population of the loggerhead shrike would be the best management strategy, as the species has declined drastically throughout the islands.     

Genetic impacts of Anacapa deer mice reintroductions following rat eradication

The Anacapa deer mouse is an endemic subspecies that inhabits Anacapa Island, part of Channel Islands National Park, California. We used mitochondrial DNA cytochrome c oxidase subunit II gene (COII) and 10 microsatellite loci to evaluate the levels of genetic differentiation and variation in ~1400 Anacapa deer mice sampled before and for 4 years after a black rat (Rattus rattus) eradication campaign that included trapping, captive holding and reintroduction of deer mice. Both mitochondrial and microsatellite analyses indicated significant differentiation between Anacapa deer mice and mainland mice, and genetic variability of mainland mice was significantly higher than Anacapa mice even prior to reintroduction. Bayesian cluster analysis and Principal Coordinates Analysis indicated that East, Middle and West Anacapa mice were genetically differentiated from each other, but translocation of mice among islands resulted in the East population becoming less distinct as a result of management. Levels of heterozygosity were similar before and after management. However, numerous private alleles in the founder populations were not observed after reintroduction and shifts in allele frequencies occurred, indicating that the reintroduced populations experienced substantial genetic drift. Surprisingly, two mitochondrial haplotypes observed in an earlier study of Anacapa deer mice were lost in the 20 years prior to the rat eradication program, leaving only a single haplotype in Anacapa deer mice. This study demonstrates how genetic monitoring can help to understand the re-establishment of endemic species after the eradication of invasive species and to evaluate the effectiveness of the management strategies employed.     

Population structure of loggerhead shrikes in the California Channel Islands

The loggerhead shrike (Lanius ludovicianus), a songbird that hunts like a small raptor, maintains breeding populations on seven of the eight California Channel Islands. One of the two subspecies, L. l. anthonyi, was described as having breeding populations on six of the islands while a second subspecies, L. l. mearnsi, was described as being endemic to San Clemente Island. Previous genetic studies have demonstrated that the San Clemente Island loggerhead shrike is well differentiated genetically from both L. l. anthonyi and mainland populations, despite the fact that birds from outside the population are regular visitors to the island. Those studies, however, did not include a comparison between San Clemente Island shrikes and the breeding population on Santa Catalina Island, the closest island to San Clemente. Here we use mitochondrial control region sequences and nuclear microsatellites to investigate the population structure of loggerhead shrikes in the Channel Islands. We confirm the genetic distinctiveness of the San Clemente Island loggerhead shrike and, using Bayesian clustering analysis, demonstrate the presence and infer the source of the nonbreeding visitors. Our results indicate that Channel Island loggerhead shrikes comprise three distinct genetic clusters that inhabit: (i) San Clemente Island, (ii) Santa Catalina Island and (iii) the Northern Channel Islands and nearby mainland; they do not support a recent suggestion that all Channel Island loggerhead shrikes should be managed as a single entity.     

Conservation genetics of an island-endemic lizard: low Ne and the critical role of intermediate temperatures for genetic connectivity

Island populations are at higher risk of extinction than mainland populations. Therefore, understanding the factors that facilitate connectivity is particularly pressing for the conservation of island taxa. Sceloporus occidentalis becki, the Island Fence Lizard, is an endemic taxon restricted to the Northern Channel Islands, part of a nearshore archipelago in Southern California, USA. Since the Last Glacial Maximum, fence lizard habitat on the Northern Channel Islands has decreased with rising sea levels and increasing temperatures that have reduced the availability of woody vegetation. More recently, the introduction (and subsequent removal) of invasive ungulates over the last 170 years and recovery of vegetation has resulted in further dramatic habitat modification. Given the potential for genetic bottlenecks, the history of habitat alteration, and topographic and landscape complexity, we used landscape and population genetic approaches to characterize patterns of genetic diversity and structure of Island Fence Lizards on Santa Cruz Island, the largest of the Northern Channel Islands. Our analyses revealed shallow population structure across the island, low effective population size (N_e?=??~?200), and evidence for a recent genetic bottleneck. Landscape genetic analyses showed that connectivity is facilitated by tree canopy cover and shrubland, as well as by intermediate temperatures, emphasizing the importance of woody vegetation and habitats with variable thermal regimes as the climate warms. Combined, these population and landscape genetic analyses suggest that the Island Fence Lizard is of greater conservation concern than currently appreciated, and increased conservation management focus is warranted for this island endemic.

     

Spatial and temporal variation in the seroprevalence of canine heartworm antigen in the island fox

Island foxes (Urocyon littoralis) are endemic to six of the eight California Channel Islands (USA). The island fox is classified as a threatened species by the State of California, and recently three of the six subspecies have experienced abrupt population declines. As part of a continuing effort to determine the cause of the declines, we tested island fox serum samples collected in 1988 (n = 176) and 1997-98 (n = 156) over the entire geographic range of the species for seroprevalence of canine heartworm (Dirofilaria immitis) antigen. Using a commercially available enzyme-linked immunosorbent assay (PetChek, Idexx Laboratories, Westbrook, Maine, USA) we detected heartworm antigen in four of the six populations of island foxes. On San Miguel and Santa Rosa Islands, seroprevalence in adult foxes was >85% (n = 62) in 1988 and increased to 100% (n = 24) in 1997-98. On Santa Cruz Island, seroprevalence in adult foxes decreased from 83% (n = 30) to 58% (n = 26), whereas on San Nicolas Island, seroprevalence increased from 25% (n = 32) to 77% (n = 30) during the same period. All of the pups assayed (n = 33) were seronegative. The seroprevalences of heartworm reported herein for the four populations of island foxes are the highest yet reported for a fox species. However, additional demographic data reported elsewhere suggests that heartworm has not been a major factor in the recent declines of island fox populations.     

RAPID MORPHOLOGICAL CHANGE IN CHANNEL ISLAND DEER MICE

Deer mice, Peromyscus maniculatus, collected over 90 years from three California Channel Islands, were examined for evidence of morphological change. Rapid morphological change has occurred in the endemic subspecies from Santa Barbara (P. m. elusus), Anacapa (P. m. anacapae), and Santa Cruz Island (P. m. santacruzae). Data were divided into two temporal classes, 1897–1941 and 1955–1988. Of the 16 morphological characters measured, between five and 10 measures changed significantly (P ? 0.05) with temporal class in each subspecies, and multivariate test statistics were significant (P ? 0.05) for all three subspecies. For each subspecies, depth of braincase, total length, tail length, and hind foot length became smaller over time, except depth of braincase, which became larger in P. m. elusus. The rates of change dramatically exceed those estimated from paleontological records and are even higher than those reported in some experimental selection studies. Temporal change in two characters exceeds differentiation between subspecies. Although changing, each subspecies remained well differentiated, and incorporation of temporal change allowed correct classification of most specimens. Unlike nearly all previous reports of rapid evolution, the changes in these populations were not associated with a founder events or recent introductions. This study demonstrates that rapid phenotypic change can occur in long-established natural populations and temporal stability of morphological characters in such populations, even over short evolutionary time periods, cannot be assumed.     

The extent of clonality and genetic diversity in the Santa Cruz Island ironwood, Lyonothamnus floribundus

Lyonothamnus floribundus , or island ironwood, is a relictual endemic species found on only four of the eight California Channel Islands. It has been suggested that this species is capable of clonal growth, although the extent of clonality has not been determined. We have used random amplified polymorphic DNA (RAPD) analysis to examine clonality and genetic diversity in L. floribundus . We found that groves are largely genetically distinct clones, indicating that they are not remnants of a once larger clonal forest. Our data also indicate that the population size of L. floribundus on Santa Cruz Island is closer to 1125 individuals, rather than 32 000 based on the number of trunks. The extensive clonality in this species may have a severe impact on its ability to reproduce sexually owing to limitation of pollinator movements among flowers within a single individual. In addition, our data indicate that the two subspecies of L. floribundus are very closely related rather than being two distinct lineages dating to the Miocene, as indicated by the fossil record.     

A new species of White‐eye Zosterops and notes on other birds from Vanikoro,Solomon Islands

A new species of white‐eye, the Vanikoro White‐eye Zosterops gibbsi, is described from the island of Vanikoro (= Vanikolo) in the Santa Cruz Islands (= Temotu Province) within the Solomon Islands. It differs from the geographically closest white‐eye, the Santa Cruz White‐eye Zosterops sanctaecrucis, by a number of features including a much longer bill, and different leg‐ and eye‐ring colour. This is the second bird species endemic to Vanikoro; the neighbouring Nendo Island supports three endemic species. Although the conservation status of this species appears to be secure, the Santa Cruz Islands are very poorly known. Despite supporting several globally threatened species, the Islands at present are not protected by any conservation activity.     

A cautionary tale on ancient migration detection: mitochondrial DNA variation in Santa Cruz Islands,Solomon Islands

Over the past decade, the origin of the first Malayo-Polynesian settlers of the island Pacific has become a contentious issue in molecular anthropology as well as in archaeology and historical linguistics. Whether the descendants of the ancestral Malayo-Polynesian speakers moved rapidly through Indonesia and Island Melanesia in a few hundred years, or whether they were the product of considerable intermingling within the more westerly part of the latter region, it is widely accepted that they were the first humans to colonize the distant Pacific islands beyond the central Solomon Islands approximately 3,000 years ago. The Santa Cruz Islands in the Eastern Solomons would have most likely been the first in Remote Oceania to be colonized by them. Archaeologically, the first Oceanic Austronesian settlement of this region appears to have been overlain by various later influences from groups farther west in a complex manner. Molecular anthropologists have tended to equate the spread of various Austronesian-speaking groups with a particular mitochondrial variant (a 9-base-pair [bp] deletion with specific D-loop variants). We have shown before that this is an oversimplified picture, and assumed that the Santa Cruz situation, with its series of intrusions, would be informative as to the power of mitochondrial DNA haplotype interpretations. In the Santa Cruz Islands, the 9-bp deletion is associated with a small number of very closely related hypervariable D-loop haplotypes resulting in a star-shaped Bandelt median network, suggesting a recent population expansion. This network is similar to Polynesian median networks. In a pairwise mismatch comparison, the Santa Cruz haplotypes have a bimodal distribution, with the first cluster being composed almost entirely of the 9-bp-deleted haplotypes-again attesting to their recent origins. Conversely, the nondeleted haplogroups bear signatures of more ancient origins within the general region. Therefore, while the profiles of the two sets of haplotypes indicate very distinctive origins in different populations with divergent expansion histories, the sequence of their introduction into the Santa Cruz Islands clearly does not follow simply.     

Distribution of Xantus' Murrelet Synthliboramphus hypoleucus at sea in the Southern California Bight, 1995–97

We radiomarked 153 Xantus' Murrelets Synthliboramphus hypoleucus captured at sea near Santa Barbara Island (SBI), the largest murrelet colony in the California Channel Islands, USA. We tracked these radiomarked murrelets in the Southern California Bight (SCB) off coastal southern California during the 1995-97 breeding seasons. In 1995 during mild El Niño conditions, the murrelets were distributed in non-upwelling areas. In 1996-97, they were distributed in dense patches, aggregating in cool upwelled waters near the northern Channel Islands or south of San Nicolas Island. Murrelets flew longer distances from SBI to foraging areas in 1997 (̄= 111 ± 44 km) than in 1996 (̄= 62 ± 25 km), but the distances they travelled did not differ between months (Apr and May) within years. Mean foraging distances from SBI were similar for 'incubating' murrelets (determined on the basis of repeated visits to SBI) and 'non-incubating' murrelets during the colony attendance period. We attributed the low return rate of radiomarked murrelets to SBI to the capture and marking of a large proportion of birds that were not actively incubating rather than to any adverse effects of radio attachment. We believe changes in murrelet foraging patterns between the 1970s and 1990s are associated with changes in prey resources in the SCB. Flexibility in the foraging strategies of these murrelets may be related to the highly variable marine environment at the southern end of the California Current Up welling System.     

Barriers to gene flow in Embiotoca jacksoni, a marine fish lacking a pelagic larval stage

Abstract.— Marine species generally show high dispersal capabilities, which should be accompanied by high levels of gene flow and low speciation rates. However, studies that focused on the relationship between dispersal and gene flow in marine fishes have been inconclusive. This study focuses on the black surfperch, Embiotoca jacksoni , a temperate reef fish that lacks a pelagic larval stage and lives on almost continuous reefs along the California and Baja California coasts. Mitochondrial control-region sequences from 240 individuals were obtained, and phylogeographic patterns were analyzed. A major phylogeographic break was found at Santa Monica Bay, a sandy expanse that prevents adult dispersal. Deep water separating the southern California Channel Islands was also found to be a major barrier to gene flow. Minor phylogeographic breaks were also detected in the Big Sur/Morro Bay and in the Punta Eugenia/Guerrero Negro regions, but none in the Point Conception region. Gene flow levels in E. jacksoni were found to be almost identical to those of another species with limited dispersal, Acanthochromis polyacanthus , thus indicating that the lack of a pelagic larval stage combined with barriers to adult dispersal may have had similar effects on these two species.     

Phenotypic variation among populations of Atherinops affinis(Atherinopsidae) with insights from a geometric morphometric analysis

Morphological character variation was examined in Atherinops affinis , a temperate marine silverside with a broad geographic range and presumed limited powers of dispersal. Populations of this species were sampled from three California mainland sites, one Channel Island site and one site in the upper Gulf of California. A geometric morphometric analysis yielded higher resolution in the assessment of phenotypic divergence among the four Pacific coast populations than either body measurement or meristic analysis, and it showed that most of the shape variation among these populations occurs in the head region and body depth of the fish. All three analyses supported the hypothesis that populations of A. affinis from central and southern California coastal waters and from Santa Catalina Island are morphologically distinct from each other; the Santa Catalina Island population was found to be the most divergent. On the basis of meristic characters alone, the population of A. affinis from the upper Gulf of California was different from A. affinis populations along the Pacific coast of California. The analyses revealed variation in several morphological characters, e.g . body depth and meristics, known to vary in association with environmental conditions. Given that A. affinis appears to have low among‐population genetic variation, this species may be phenotypically plastic in response to the environmental conditions of the habitat of each population.     

Eelgrass meadows in the California Channel Islands and adjacent coast reveal a mosaic of two species, evidence for introgression and variable clonality

BACKGROUND AND AIMS: Seagrasses are important facilitator species in shallow, soft-bottom marine environments worldwide and, in many places, are threatened by coastal development and eutrophication. One narrow-leaved species (Zostera marina) and one wide-leaved species, variously designated as Z. marina, Z. pacifica or Z. asiatica, are found off the California Channel Islands and adjacent California-Mexico coast. The aim of the present study was to confirm species identification genetically and to link patterns of genetic diversity, connectivity and hybridization among and within the populations with historical sea levels (Ice Age) or the contemporary environment. METHODS: Samples (n = 11-100) were collected from 28 sites off five California Channel Islands and six sites off the adjacent coast of southern California and Baja California, Mexico. DNA polymorphisms of the rDNA-ITS (internal transcribed spacer) cistron (nuclear), the matK intron (chloroplast) and nine microsatellite loci (nuclear) were examined in a population genetic and phylogeographic context. KEY RESULTS: All wide-leaved individuals were Z. pacifica, whereas narrow-leaved forms were Z. marina. Microsatellite genotypes were consistent with hybridization between the two species in three populations. The present distribution of Z. pacifica follows a glacial age land mass rather than present oceanographic regimes, but no link was observed between the present distribution of Z. marina and past or present environments. Island populations of Z. marina often were clonal and characterized by low genotypic diversity compared with populations along the Baja California coast. The high level of clonal connectivity around Santa Catalina Island indicated the importance of dispersal and subsequent re-establishment of vegetative fragments. CONCLUSIONS: The pristine environmental conditions of offshore islands do not guarantee maximum genetic diversity. Future restoration and transplantation efforts of seagrasses must recognize cryptic species and consider the degree of both genetic and genotypic variation in candidate donor populations.     

Exome sequencing of deer mice on two California Channel Islands identifies potential adaptation to strongly contrasting ecological conditions

Understanding the forces that drive genotypic and phenotypic change in wild populations is a central goal of evolutionary biology. We examined exome variation in populations of deer mice from two of the California Channel Islands: Peromyscus maniculatus elusus from Santa Barbara Island and P. m. santacruzae from Santa Cruz Island exhibit significant differences in olfactory predator recognition, activity timing, aggressive behavior, morphology, prevalence of Sin Nombre virus, and population densities. We characterized variation in protein‐coding regions using exome capture and sequencing of 25 mice from Santa Barbara Island and 22 mice from Santa Cruz Island. We identified and examined 386,256 SNPs using three complementary methods (BayeScan, pcadapt, and LFMM). We found strong differences in molecular variation between the two populations and 710 outlier SNPs in protein‐coding genes that were detected by all three methods. We identified 35 candidate genes from this outlier set that were related to differences in phenotypes between island populations. Enrichment analyses demonstrated that patterns of molecular variation were associated with biological processes related to response to chemical stimuli and regulation of immune processes. Candidate genes associated with olfaction (Gfy, Tlr2, Vmn13r2, numerous olfactory receptor genes), circadian activity (Cry1), anxiety (Brca1), immunity (Cd28, Eif2ak4, Il12a, Syne1), aggression (Cyp19a, Lama2), and body size (Bc16, Syne1) exhibited non‐synonymous mutations predicted to have moderate to large effects. Variation in olfaction‐related genes, including a stop codon in the Santa Barbara Island population, suggests loss of predator‐recognition traits at the molecular level, consistent with a lack of behavioral aversion to fox feces. These findings also suggest that divergent pathogen prevalence and population density may have influenced adaptive immunity and behavioral phenotypes, such as reduced aggression. Overall, our study indicates that ecological differences between islands are associated with signatures of selection in protein‐coding genes underlying phenotypes that promote success in those environments.