Genetic monitoring in California State Parks: Potential for including genetic sampling as part of the IMAP and for consequently improving genetic management of native species

Rogers, D.L., R.A. Woodward, P.E. McGuire, S.K. Brown, D.R. Elam, H.B. Ernest, E.R. Heeg, J.M. Hull, L.S. Kimsey, K.J. Rice, H.B. Shaffer, B.N. Sacks, R.S. Schwartz, and J.A. Well

Prepared with funding from the California Department of Parks and Recreation through Interagency Agreement # C0218001 with the Genetic Resources Conservation Program, University of California

Summary and recommendations
Introduction
What genetic monitoring can potentially indicate
Comments on collecting biological samples for genetic assessment
Interpreting genetic information
Opportunities and priorities for genetic monitoring in Cal Parks
Abstracts of presentations
Rogers | Elam | Rice | Kimsey | Ernest et al. | Schwartz and May | Shaffer
Cited and selected literature related to genetic monitoring
Workshop participants

Summary and recommendations

On February 16, 2005 the California Department of Parks and Recreation (DPR) sponsored and co-organized, with the Genetic Resources Conservation Program of the University of California, a workshop on genetic monitoring. Attended by mainly UCD researchers who conduct genetic studies on California native plants and animals, together with individuals from agencies and organizations that manage or contribute to the conservation of these taxa, the objective was to discuss the opportunity for including genetic monitoring as part of the Inventory, Monitoring & Assessment Program (IMAP) of the DPR. Presentations illustrated the various kinds of information that could be gained from genetic monitoring, how monitoring methods and timeframes would vary according to general taxonomic groups, the different kinds of genetic information and what they reflect, and how contextual information (species characteristics, spatial and temporal environmental information) is critical for appropriately interpreting genetic information. Although formal recommendations were not put forward by the group, several points emerged from discussions that can be framed as informal recommendations:

  1. It is neither reasonable nor feasible to collect biological samples towards a goal of genetically monitoring all taxa—or even all plant and animal taxa—in State Parks. However, in some situations, genetic monitoring is well recommended for the information that it can provide towards identifying potential problems or more effective conservation. Priorities could include: listed species; species that have recently undergone severe habitat reduction, habitat fragmentation, or loss of census size; populations suspected of possible hybridization with introduced conspecific populations or sexually compatible species; or species that may reflect environmental quality or contamination.
  2. Prior to collecting samples for genetic monitoring, it is advisable to contact a researcher who conducts (or has conducted) genetic studies on the species of interest or a related species. This can serve three purposes: i) Provide information on sampling protocol, including season, timeframe, and methods for sampling (Genetic monitoring is difficult to reduce into a standard protocol. It varies according to both objective and the species under consideration); ii) Ensure there is an interested researcher to receive, store, analyse, and interpret the samples; and iii) Ensure the information (research results, DNA sequence information, etc.) is shared and stored appropriately (e.g., Genbank, Natural Diversity Database, USGS’s Biological Information Observation System (BIOS), etc.).
  3. For genetic monitoring, it is just as essential to collect environmental information (e.g., sample location, site description) as it is the biological sample itself. This is critical for meaningful interpretation of the genetic data.
  4. Insects are a special case: although for most insect species there is probably not enough basic information to support genetic monitoring, monitoring on a species (or higher taxonomic level) is very important. There are major blackholes in our knowledge of California insects and yet they play critical ecological (and agricultural) roles. Considerable taxonomic expertise is required for monitoring insect species. It is recommended that this expertise be incorporated, where possible, into training for IMAP so that the diversity and health of insect populations (as well as potential threats from invasives) can be better monitored.
  5. There is a need for coordinated efforts for seed collections, inventories, and biological collections to support effective genetic monitoring. A directed workshop (and suitable actions following from that) is recommended.
  6. In addition to determining more information about the populations and species of interest, genetic monitoring can be used, in specific cases, to indicate changes in environmental condition or quality. For this reason, priorities for genetic monitoring should also consider environmental areas of concern or interest, in addition to the species themselves.

Introduction

The California Department of Parks and Recreation (hereafter called ‘Cal Parks’) has recently expanded and revised their monitoring program for plant and animal taxa in State Parks: the Inventory, Monitoring & Assessment Program (IMAP). A workshop (‘Genetic monitoring in California State Parks: Improving connections between species management and genetic research’) was conducted on February 16, 2005 to provide an opportunity to explore the idea of including some genetic aspects to IMAP activities-making additional observations or collections as part of IMAP field activities that would contribute to genetic research; providing information on the genetic nature of species that would have implications for the monitoring program; or any other ideas that would contribute to increasing the information gained through IMAP, particularly about the genetic diversity of species. The objectives were to provide Cal Parks (and other interested and participating agencies and organizations) with some ideas about the utility/application of genetic monitoring for various taxa, to provide selected genetic researchers with information about the State Parks monitoring program, and to discuss ideas for how the Cal Parks inventory/monitoring program might include genetic monitoring and enhance research. The workshop was initiated, funded, and co-organized by Cal Parks (Dr. Roy Woodward) and was co-organized and hosted by the Genetic Resources Conservation Program of the University of California (Drs. Deborah Rogers and Patrick McGuire).

Genetic monitoring refers to assessment of genetic diversity over time. Other types of genetic studies may investigate genetic relationships among species or subspecies or the relationship between the genetic diversity of a species and the way it is structured spatially across the species’ range. Genetic monitoring implies a temporal component to the study. The appropriate timeframe for sampling genetic diversity to detect meaningful changes will vary according to species (for example, the length of their individual lifespans: in general, the longer lived the species and the longer the time to reproductive maturity, the longer it will take in absolute time to detect genetic changes) and to the environment (for example, how quickly the environment is changing or the presence and severity of human influences such as habitat loss or environmental degradation). Biologically meaningful changes in the genetic diversity of a species occur over generations of that species, rather than within the lifetimes of individuals.

What genetic monitoring can potentially indicate

Within the context of natural areas management, there are two main uses of genetic monitoring: to determine genetic responses of species to severe environmental contamination (e.g., increased mutation rate in response to a major pollution event; for example, see Lavie and Nevo 1987) and to detect genetic changes over time in native populations that may be in response to more gradual or cumulative changes in the environment—either natural or human-influenced. The interest here is on the latter category.

Monitoring the genetic diversity of populations of native species over time can be useful in detecting situations or trends that may confirm normal levels of diversity or alert managers to potential problems. Examples of situations that can be detected with genetic monitoring include the following:

  1. Loss of genetic diversity: Monitoring can detect biologically significant changes in genetic diversity over time. Large losses in diversity could have negative effects on fitness and survival in the long term, and ability to adapt to changing environmental conditions.
  2. Genetic structure (or loss of genetically differentiated populations): In addition to the spatial pattern of genetic diversity in a species (e.g., how well differentiated or similar are the various populations or regions of a species), monitoring can track changes in this structure over time, indicate a metapopulation structure, or detect a trend towards loss of a population (prior to actual decrease in census number).
  3. New hybridizations: Hybridizations between subspecies or species, such as those between reintroduced populations or between native and exotic species, can be detected.
  4. Effects of fragmentation: Genetic impacts can result from fragmentation of habitat. In outbreeding plants, for example, major fragmentation of habitat can lead to an increase in inbreeding and possibly inbreeding depression.
  5. Has population undergone a bottleneck: Genetic monitoring can determine whether the population has gone through a severe reduction in census size in the usually distant past, regardless of current size. This history can have implications for the genetic diversity and viability of the population.
  6. Susceptibility to disease: In some cases, genetic diversity can indicate susceptibility to disease. For example, there may be genetic resistance that can be determined; certain genetic conditions (e.g., inbreeding depression) may make a population more susceptible to contracting or suffering the effects of introduced diseases.
  7. Gender ratio (in absence of sexual dimorphism): Sexual identity and gender ratios can be determined by genetic analysis, even when this is not apparent from morphological traits.
  8. Clones, family structure/relationships: The genetic relationship among individuals can be determined from genetic studies. This can be particularly important in small populations where inbreeding depression could be a concern.
  9. Genetic contamination: If nonlocal plant materials or animals are introduced to an area, breeding with the native population(s) could potentially undermine local adaptations in the long term.
  10. Domestic - wild populations (interbreeding, assimilation): The degree to which domesticated individuals (e.g., landscaping plants, hatchery fish, farm animals) are interbreeding with native wild populations can be determined by genetic studies.

Comments on collecting biological samples for genetic assessment

Various kinds of tissues can be used to obtain DNA for genetic analysis. This can be done nondestructively in most cases—that is, without harm or discomfort (in the case of animals). Depending on the species and situation, road-killed animals may be valuable sources of genetic information. However, the type of tissue most useful, the amount of tissue needed, and even storage conditions may vary from species to species or at least among major taxonomic groups. For example, seeds of conifer species (e.g., pines) contain different kinds of genetic information than do seeds of angiosperms (e.g., poppies or poplars). Consequently, before making a collection it is important to connect with a researcher who is familiar with the species and interested in doing a genetic study or at least in maintaining a collection of tissues or extracted DNA, so that specific sampling and transport/storage information can be obtained. Some generalizations include:

  1. Formalin is not recommended for storing tissue samples.
  2. Depending on tissue type, the stability of the protein or DNA may be affected by certain temperature or moisture conditions. The sensitivity of samples to changes in moisture (either too much humidity or desiccation) and temperature extremes should be determined. In addition, the optimum transport time (from field collection to reception by researcher) should be known.
  3. Environmental information should be collected in concert with vouchers.
  4. The identity of the sample should be maintained at all times and full records should be kept (redundancy is desirable).

Interpreting genetic information

Because of the different types of genetic diversity and the various statistical and mathematical methods to analyse them, genetic information requires considerable context and expertise for appropriate interpretation. In general:

  1. Genetic information needs biological context for meaningful interpretation (e.g., implications of sample size; limitations of method/data type; environmental influences; management effects; genome context (different implications of mtDNA, cpDNA, nuclear DNA); controls or baseline data).
  2. One type of genetic data or genetic method of analysis is not necessarily better than others: however, each has appropriate uses and also limitations.
  3. In some cases (especially where the outcome of a genetic monitoring project could have serious economic or political outcomes) peer review of the genetic information (i.e., interpretation by various, appropriate researchers) may be needed to ensure that the appropriate biological context has been provided and to approach objectivity in interpretation.
  4. If a genetic monitoring study does not provide evidence of genetic differentiation (e.g., among populations), this result may be related to methods.
  5. Ubiquitous distribution and high mobility does not necessarily mean there will be no spatial genetic structure in a species (e.g., coyotes: see the presentation abstract by Holly Ernest and colleagues, below).
  6. Patterns revealed by genetic monitoring require careful interpretation in their relation to historical versus current or ongoing influences. There can be a significant lag effect in genetic information reflecting event (e.g., cessation of gene flow; see Slatkin and Barton 1989).
  7. ‘Neutral genetic variation’ does not mean unimportant genetic variation. Rather, it means genetic variation that is not under the influence of natural selection.

Opportunities and priorities for genetic monitoring in Cal Parks

It is not realistic (or reasonable) to monitor genetic diversity in all taxa in California State Parks. But there are some taxa or situations that would greatly benefit from the information provided by genetic monitoring. Also, there are some good research opportunities/situations where genetic monitoring might provide some valuable insights, including:

  • Wild populations—e.g., populations at periphery of natural ranges (could be small populations at risk, locally adapted populations, populations with valuable genetic diversity in responding to climate change, etc.); species or populations that have experienced recent and rapid decreases in size; species or populations that have experienced rapid habitat loss or fragmentation; listed species.
  • Restored populations—where genetic monitoring is critical to predict the success of the restoration.
  • Species or populations that are in particular areas where there is concern about responses to particular environmental events or influences.
  • Research opportunities—e.g., long-term studies with one sampling event (overlapping generations—e.g., coast redwood, giant sequoia; soil or canopy seed banks).

Abstracts of presentations

Rogers | Elam | Rice | Kimsey | Ernest et al. | Schwartz and May | Shaffer


“Genetic monitoring in California State Parks: Improving connections between species management and genetic research”—Deborah Rogers (Genetic Resources Conservation Program, University of California)

Questions that relate to genetic monitoring with the California State Parks system and are within the scope of this workshop include:

  • How to make biological collections and monitoring more biologically meaningful?
  • How to incorporate genetic information into monitoring activities?
  • How to collect genetic information?
  • Which taxa might be most appropriate for genetic monitoring?
  • What can genetic monitoring tell us?
  • How to share and coordinate biological collections?

Genetic monitoring is difficult to reduce into a standard protocol. It varies according to both objective and the species under consideration. For each objective and species, the following questions can then be raised to help determine an appropriate monitoring protocol:

  • What is the appropriate time-scale to detect significant genetic change?
  • What genetic measures are appropriate?
  • What is the appropriate (spatial, seasonal, etc.) sampling design?
  • What genetic attribute (derived from the genetic data) is the most effective to capture the potential genetic change (Effective population size? Diversity? Genetic structure?)?

It is reasonable to consider monitoring genetic diversity in some cases, because of the importance of genetic diversity to species’ fitness, evolutionary potential, ability to occupy new ecological niches, and potential to respond to environmental change. See Reed and Frankham (2003) for evidence of a significant and positive relationship between genetic diversity and fitness across a broad range of taxa.

Genetic diversity is dynamic, constantly being influenced by natural processes. These processes include natural selection, random genetic drift, and gene flow. Consequently, genetic monitoring studies or programs are best designed with the timeframe, direction, and general influence of these processes in mind, so as to allow detection of genetic changes that are from other sources (e.g., habitat loss or direct species loss, unnatural hybridizations or genetic contamination from nonlocal introduced or planted populations, etc.). A proper ‘background of genetic variation’ is important to establish to enable detection of unusual or undesirable changes.

Genetic monitoring can provide information that normal census data may not, for example:

  • In some species (lacking sexual dimorphism), sex identification; gender ratio in a population
  • Clone identification in species that reproduce asexually
  • Family relationships among individuals
  • Dramatic changes in population size over time (that have occurred historically, and for which there is still a record in the genetic diversity of the populations)
  • Population dynamics (gene flow/migration among populations, evidence of local adaptations, etc.)
  • Hybridizations among subspecies or species
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“Use of genetics and monitoring in FWS Recovery Plans: Observations and case studies”—Diane Elam (US Fish and Wildlife Service, Sacramento, CA)

A search (using the California Natural Diversity Database and the Department of Parks and Recreation (R.A. Woodward, pers. com.)) revealed that approximately 24 plant taxa and 21 animal taxa that occur on California State Parks are federally listed. Among the listed plant taxa, recovery plans for 12 recommended preserving genetic material ex situ (seed collections, greenhouse populations) and 10 recommended genetic studies (patterns of genetic diversity, limiting genetic factors, systematics, clonality, hybridization). For example, the endangered Eriodictyon altissimum is known from six locations, two of them in Montaña de Oro State Park. Both this species, and the endangered Lompoc yerba santa (Eriodictyon capitatum), can reproduce vegetatively, so genetic studies would be useful in determining the extent of genetic diversity and size/number of clones. Genetic research has been recommended for the endangered Cupressus abramsiana to determine whether, or to what extent, hybridization with native cypresses has occurred. For six plant taxa, FWS recovery plans indicated introductions or supplementations of native material. Genetic studies could help determine the most appropriate sources of plant material and help determine any impacts on the native populations. For only one of the listed plant species was genetic monitoring recommended—the Otay tarplant (Deinandra conjugens). This threatened species, present at Anza-Borrego Desert State Park, is self-incompatible. Incompatibility is controlled by the ‘S-locus’ and individual plants are only sexually compatible if they have different alleles at this locus. The recommended study involves determination of the S-allele variation, identification of isolated populations that may need augmentation, identification of genetic augmentation techniques, monitoring genetic variability, and research to identify limiting genetic factors.

Of the 21 listed animal species in State Parks, recovery plans for seven indicated preserving genetic material ex situ (captive propagation). Examples include the California condor and the riparian brush rabbit. For 14 of the listed animal taxa, recovery actions included recommendations for genetic research to determine patterns of genetic diversity, relationship with other species/taxa, or hybridization issues. For some species—including peninsular bighorn sheep and desert pupfish—genetic monitoring was recommended.

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“Can we link ecological monitoring with evolutionary processes? or Genetics ‘on the cheap’”—Kevin Rice (Department of Plant Sciences and Center for Population Biology, UCD)

Genetic differences among or between populations of a species may represent differences in local adaptations. There is also genetic diversity within each of the populations—that diversity represents potential to adapt to new environmental conditions in the future.

There are various kinds of genetic diversity and many ways to measure it. Some genetic diversity represents adaptation; some is ‘neutral’-meaning that it is (or assumed to be) not influenced by natural selection. However, ‘neutral’ genetic variation should not be misconstrued as unimportant. It simply is not currently and apparently influenced by selection. These different types of genetic diversity are not necessarily correlated with one another. Consequently, it is important to interpret genetic diversity measures carefully, as each may tell us a different part of the story, and one is not necessarily better than the other, but simply more appropriate for answering different types of questions. Furthermore, there is a lag between the influence on genetic diversity (e.g., cessation of gene flow between two populations, or the beginning of a new type or degree of natural selection) and its reflection in the DNA or other diversity measures.

The different natural processes that influence the amount and pattern of genetic diversity in native populations include mutation, natural selection, genetic drift, and migration (gene flow). Natural selection and genetic drift tend to increase the genetic differentiation among populations; gene flow among populations tends to homogenize differences.

Inbreeding depression can result when previously outcrossing individuals are restricted in their breeding activities and mate with relatives. At the genetic level, this means that alleles (i.e., one copy of a gene) that previously were deleterious but recessive (i.e., ‘cloaked’ by being paired with a beneficial or neutral allele that was dominant) are now more likely to co-occur. When that happens (i.e., two recessive deleterious alleles are paired), the deleterious effect is expressed. Collectively, this can lead to lower viability and fitness in the long term. This chain of events happens more quickly in small populations.

The census size of a population (the total number of individuals) and its ‘effective’ population size (the number of individuals involved in reproduction) are often not the same. Unequal gender ratios (in animal species and dioecious plant species), fluctuating population sizes from one generation to another, and other influences can cause the effective size to be much smaller than the census size.

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“Insects: Good, bad, & ugly—Should we care?”—Lynn Kimsey (Department of Entomology and the Bohart Museum of Entomology, UCD)

Insects are small but they dominate habitats. E.O. Wilson estimated that in the US there are 400 lbs of insects relative to 14 lbs of humans per acre! There are many different insect species or taxa: in fact, there are more kinds of insects than any other group of animals or plants (see Purvis and Hector 2000). However, many insects have not yet been documented or, if named, they still remain largely unknown. The number of insects with common names is less than 0.001% of the total species. Insects also have major impacts on other species and on ecosystem functioning. Every insect species has at least one species of insect parasite. Among the vast number of insect species, there is an amazing variety of biologies: mosquitoes and houseflies can have a new generation every two weeks during warm weather; jewel beetles spend 1 to 10 years in a larval stage; mayflies live one year as a larva and three days as an adult; monarch butterflies live two to three years as adults and three months as larvae; aphids are born pregnant. There is also immense diversity in reproductive potential: one aphid can produce 10108 descendents in her lifetime; monarch butterflies produce only about 20 offspring. This diversity of life histories also illustrates the potential complexity of any monitoring program. For example, the frequency of monitoring would vary greatly depending on the generation times of the species studied, and what would be monitored would depend on the life stages and time spent in each stage.

In California, there are an estimated 100,000 species of insects. Of these, 12% are endemic, 9% are new to science, and in some habitats up to 70% may be exotic. California is particularly rich in insect species, with 500 insect families occurring here, with only 600 families in all of North America. In South America, there are about 900 families of insects known. There are various distribution patterns for California insects; some are based on geography or environmental conditions (e.g., a west-east gradient, with the number of families of insects increasing as you move inland from the coast), others are based on research foci (that is, there are distributions that reflect the work from particular research programs or researchers), and others are related to the location of programs that monitor for insects. There are large blackholes in our knowledge of insects, and entire counties or habitat types in California for which we know little about the insect species.

Insect species play a diversity of important ecosystem roles-as food, pollinators (i.e., most plants need insect pollinators; endangered plants may have only one insect pollinator), disease vectors, and recyclers (i.e., as wood feeders, detrivores, carrion feeders, and scavengers). They can also be bioindicators of environmental quality as they are fine-tuned to the environment. For example, shifts in insect populations or species can indicate acid mine run-off (e.g., as indicators of changes in pH), contamination from such sources as livestock or sewage, or even activities such as marijuana plantations (related to sharp changes in certain nutrients). In particular, aquatic insects can be excellent bioindicators as they have very specific water quality requirements (and thus changes in species would reflect changes in conditions) and they are easy to sample. However, taxonomic expertise is required for such monitoring.

Monitoring insect populations, consequently, can not only provide more information directly on these species, but provide information on indirect impacts on other species, environmental quality, and new exotics that might become invasive and problematic. To make insect monitoring feasible and useful, additional taxonomic expertise (more entomologists) and training of field staff are needed.

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“Genetic monitoring of wildlife: Mammals and birds”—Holly Ernest, Ben Sacks, Joshua Hull, Sarah Brown, Elizabeth Heeg, and Jay Well (Wildlife & Ecology Unit, Veterinary Genetics Laboratory, UCD)

Genetic monitoring of wildlife populations in California can contribute information useful to protecting their health, conserving their long-term viability, and providing management options. As most species studied by the Wildlife & Ecology Unit are wide ranging, the studies cross multiple states and sometimes country borders. Genetic monitoring of the yellow-billed magpie (Pica nutalli) is focused on determining the current level of genetic diversity, population genetic structure, and the relationship—if any—between genetic diversity and structure and the observed decline in the numbers of birds. Similarly, genetic studies of the Swainson's hawk (Buteo swansoni), red-tailed hawk (Buteo jamaicensis), and the great gray owl (Strix nebulosa) seek information on the genetic relationship among populations-whether certain populations are distinct and the level and direction of gene flow among them. A genetic study of coyote populations in California revealed a diverse pattern of population relationships: some genetically distinct populations in the south and central coast areas of California, continuous (i.e., high gene flow) populations in northern and eastern California, and moderate gene flow (moderate genetic similarity) between east-west populations in the northern and southern regions of the Central Valley. In general, although coyotes have been previously described as ubiquitous in California and assumed to be fairly wide ranging (and consequently expected to have mid- to high levels of gene flow), genetic studies suggest there are habitat-specific genetic subdivisions statewide. Additional samples are currently being collected from southern California. Ongoing studies for the red fox and black bear are seeking information on population genetic structure and historical patterns of gene flow (migration).

Feral pigs in California—originating from free-range domestic pigs in the coastal region in the 1700s and from wild boars introduced into Monterey County in 1925 and the 1950s—have caused much damage to natural environments (such as oak woodlands) and to livestock (direct predator activity and transmitting diseases such as cholera, swine brucellosis, foot and mouth disease, and African swine fever). Statewide genetic studies are helping to determine genetic structure and relationship with landscape influences and how populations change over time.

Genetic analysis is also used in forensic studies of wildlife to help determine illegal activities (such as harvesting of protected species) or wildlife behavior that may impact public health or welfare (e.g., wildlife attacks, impacts to food supply). For example, genetic analysis can be useful in discriminating closely related species-a decision that is important when one of the species is endangered and protected. Genetic studies were used to determine whether a diesel fuel spill into Suisun Marsh killed, among other mammals, an endangered mouse (Reithrodontomys raviventris) or a common harvest mouse (Reithrodontomys megalotis).

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“Genetic monitoring in selected California fish and amphibians”—Rachel Schwartz and Bernie May (Department of Animal Science, UCD)

Sampling fish for genetic studies can be done nondestructively and fairly easily. After catching the fish, a small sample from a fin is removed and stored (dry) in a coin envelope or in a small plastic tube in 95% ethanol (quickly returning the fish to the water after sampling). For fish species, genetic monitoring is most commonly used to help delineate management units (by determining patterns of genetic differentiation), determine hybridization, improve restoration activities, and suggest potential health/population viability problems. For most fish species, the life expectancies of individuals and life history stages are such that sampling for genetic information would logically occur either annually (to detect changes in genetic diversity over time; over perhaps over longer periods) or twice or more per year (to detect genetically significant differences in offspring survival or differences in genetic contributions among parents). Because of the large impact of commercial salmon fishing and hatcheries, genetic studies for native salmon and trout species often focus on the genetic effects on native populations of hatchery-raised fish, hybridization between domestic and wild fish, and genetic impacts from habitat fragmentation. For example, a genetic study of California golden trout investigated the degree of hybridization between this species and rainbow trout that were released in their native habitat in Golden Trout Creek and in the lower South Fork Kern River. Genetic monitoring of the Sacramento perch—reintroduced to Suisun Marsh after becoming locally extinct—will help determine the health (e.g., genetic diversity, number of parents participating in reproduction) of the reintroduced population and whether this population is interbreeding with other native populations.

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“Genetic monitoring in some California amphibians and reptiles”—H. Bradley Shaffer (Section of Evolution and Ecology, College of Biological Sciences, UCD)

A genetic study of 84 populations of the tiger salamander (Ambystoma californiense), encompassing its entire range in California, revealed six genetically differentiated regions. Populations from Santa Barbara and Sonoma Counties are particularly well differentiated and geographically isolated from all others. These two populations are defensible as genealogical species. The geological history of California, together with the genetic evidence, suggest that the Santa Barbara population has been isolated for at least 0.74 to 0.92 million years and the Sonoma clade is equally ancient. The remaining units in the Southern San Joaquin Valley, Central Coast Range, Central Valley, and San Francisco Bay Area are separated by geological features, ecological zone boundaries, or both. In combination with previous and ongoing landscape ecological studies, this work suggests that, within units, California tiger salamanders are not particularly philopatric, but there is a deep genetic differentiation among major geographical regions (Trenham et al. 2001; Shaffer et al. 2004b; Trenham and Shaffer 2005).

Genetic studies of nuclear and mitochondrial DNA have also elucidated patterns of interspecific hybridization among native and introduced tiger salamander species. The barred tiger salamander (Ambystoma tigrinum mavortium) was introduced by bait dealers into the native range of the California tiger salamander (A. californiense). Hybridization and backcrossing have been occurring in central California for 50 to 60 years, or an estimated 15 to 30 generations. Hybridization was studied by analyzing the relative frequencies of hybrid genotypes in three kinds of breeding habitats: natural vernal pools, ephemeral man-made cattle ponds, and perennial man-made ponds. Perennial man-made ponds tended to have higher frequencies of nonnative alleles than either type of seasonal pond. This was true even in cases where perennial and seasonal ponds were within a few hundred meters of one another. This is most likely the result of differing types of natural selection between the two pond types. Thus, for these species, the hybrid zone has a mosaic structure that depends on pond hydrology or ecology (Riley et al. 2003; Fitzpatrick and Shaffer 2004).

The red-legged frog, Rana aurora, is currently recognized as one species with two subspecies, aurora and draytonii. R.a. draytonii is protected under the US Endangered Species Act. A recent genetic survey (using mitochondrial DNA) of 50 populations of red-legged frogs from across their range provided several major results. (1) Consistent with several other lines of independent evidence, aurora and draytonii are each distinct, evolutionary lineages; the mtDNA data indicate that they do not constitute a monophyletic group, but rather that aurora and R. cascadae from the Pacific northwest are sister taxa; (2) the range of the draytonii mtDNA clade extends about 100 km further north in coastal California than was previously suspected, and corresponds closely with the range limits or phylogeographical breaks of several codistributed taxa; (3) a narrow zone of overlap exists in southern Mendocino County between aurora and draytonii haplotypes, rather than a broad intergradation zone; and (4) the critically endangered population of draytonii in Riverside County, CA forms a distinct clade with frogs from Baja California, Mexico. The currently available evidence favors recognition of aurora and draytonii as separate species with a narrow zone of overlap in northern California (Shaffer et al. 2004a).

The western pond turtle, Emys marinorata, is declining throughout its range, primarily because of loss of habitat via urbanization, conversion to agriculture, and interactions with invasive turtles. Recent genetic studies across this species’ native range (Washington state to northern Baja California) have identified four distinctive groups within this species: a large northern group that includes those populations in Washington, Oregon, and northern California; a southern group (roughly, east of Santa Barbara, CA and south); a San Joaquin Valley group; and a small localized group near Santa Barbara. The identity of, and relationships among, these groups and the two recognized subspecies, E.m. marmorata and E.m. pallida, provides a more detailed framework for appropriate management strategies for conservation and restoration (Spinks et al. 2003; Spinks and Shaffer 2005).

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Cited and selected literature related to genetic monitoring

Blaustein, A.R. and D.B. Wake. 1990. Declining amphibian populations: A global phenomenon. Trends in Ecology and Evolution 5:203–204.

Cordes, J.F., M.F. Blumberg, and B. May. Identifying introgressive hybridization in native populations of California golden trout based on molecular markers. Submitted to Proceedings of the Western Division of the American Fisheries Society Symposium on Western Native Fishes.

Cordes, J.F., M.A. Blumberg, G.A.E. Gall, and B. May. 2001. Genetic status of California golden trout populations in the headwaters of Golden Trout Creek. Report to the Threatened Trout Committee, California Department of Fish and Game. September 2001. 34 pp.

Cordes, J.F., M.R. Stephens, and B.P. May. Genetic status of California golden trout in the South Fork Kern River and transplanted populations: Report to the Threatened Trout Committee, California Department of Fish and Game (in prep).

Cruden, R.W. 1977. Pollen-ovule ratios: A conservative indicator of breeding systems in flowering plants. Evolution 31:32-46.

Davidson, C., H.B. Shaffer, and M.R. Jennings. 2002. Spatial tests of the pesticide drift, habitat destruction, UV-B, and climate-change hypotheses for California amphibian declines. Conservation Biology 16:1588–1601.

Dow, B.D. and M.V. Ashley. 1996. Microsatellite analysis of seed dispersal and parentage of saplings in bur oak, Quecus macrocarpa. Molecular Ecology 5:615–627.

Dow, B.D. and M.V. Ashley. 1998. Factors influencing male mating success in bur oak, Quercus macrocarpa. New Forests 15:161-180.

Dyer, A.R. and K.J. Rice. 1997. Evidence of spatial genetic structure in a California bunchgrass population. Oecologia 112:333–339.

Dyer, A.R. and K.J. Rice. 1997. Intra-specific and diffuse competition: The response of Nassella pulchra in a California grassland. Ecological Applications 7:484–492.

Ellstrand, N.C. and D.R. Elam. 1993. Population genetic consequences of small population size: Implications for plant conservation. Annual Review of Ecology and Systematics 24:217–42.

Elam, D.R. 1998. Population genetics of vernal pool plants: Theory, data and conservation implications. pp. 180-189. in Proceedings of Conference on the Ecology, Conservation and Management of Vernal Pools. Sponsored by the California Native Plant Society. Sacramento, California.

Endangered Species Recovery Program (ESRP), Riparian brush rabbit.

Ernest, H.B., V. Bleich, B. May, S. Stiver, S. Torres, and W. Boyce. 2003. Population genetic structure of mountain lions in California. Conservation Genetics 4:353–366.

Ernest, H.B., E. Rubin, and W. Boyce. 2002. Fecal DNA analysis and risk assessment of mountain lion predation of bighorn sheep. Journal of Wildlife Management 66:75–85.

Ernest, H.B., M.C.T. Penedo, B.P. May, M. Syvanen, and W.M. Boyce. 2000. Molecular tracking of mountain lions in the Yosemite Valley region in California: genetic analysis using microsatellites and fecal DNA. Molecular Ecology 9:433–441.

Fitzpatrick, B.M. and H.B. Shaffer. 2004. Environment-dependent admixture dynamics in a tiger salamander hybrid zone. Evolution 58:1282–1293.

FWS Recovery Plans

FWS Listing Information

Gall, G.A.E., C.A. Busack, R.C. Smith, J.R. Gold, and B.J. Kornblatt. 1976. Biochemical genetic variation in populations of golden trout, Salmo aguabonita: Evidence of the threatened Little Kern River golden trout, S.a. whitei. Journal of Heredity 67:330–335.

Gordon D.R. and K.J. Rice. 1998. Patterns of differentiation in wiregrass (Aristida beyrichiana): Implications for restoration efforts. Restoration Ecology 6:166–174.

Holmes, T.H. and K.J. Rice. 1996. Life history impacts on the soil moisture dynamics of a Mediterranean herbaceous community. Annals of Botany 78:233–234.

Hopper Mountain National Wildlife Refuge, California condor.

Hufford, K.M. and S.J. Mazer. 2003, Plant ecotypes: genetic differentiation in the age of ecological restoration: Trends in Ecology and Evolution 18:147–155.

Hull J.M., D.J. Girman. 2005. Effects of Holocene climate change on the historical demography of migrating sharp-shinned hawks (Accipiter striatus velox) in North America. Molecular Ecology 12:159–170.

IMAP information.

Kimsey, L.S. 1996. Status of terrestrial insects. pp. 735–741 in Sierra Nevada Ecosystem Project, Final Report to Congress, Status of the Sierra Nevada, Volume II.

Knapp, E.E. and K.J. Rice. 1994. Genetic issues in the collection and use of native grasses for restoration. Restoration and Management Notes 12:40–45.

Knapp, E.E. and K.J. Rice. 1996. Genetic architecture and gene flow in Elymus glaucus (blue wildrye): Implications for native grassland restoration. Restoration Ecology 4:1–10.

Knapp, E. E. and K.J. Rice. 1998. Comparison of isozymes and quantitative traits for evaluating patterns of genetic variation in purple needlegrass (Nassella pulchra). Conservation Biology 12:1031–1041.

Knapp, E.E., M.A. Goedde, and K.J. Rice. 2001. Pollen-limited reproduction in blue oak: Implications for wind pollination in fragmented populations. Oecologia 128:48–55.

Lavie, B. and E. Nevo. 1987. Differential fitness of allelic isozymes in the marine gastropods Littorina punctata and Littorina neritoides exposed to the environmental stress of the combined effects of cadmium and mercury pollution. Environmental Management 11:345–350.

Linhart, Y.B. 1995. Restoration, revegetation, and the importance of genetic and evolutionary perspectives. in Rotundy, B.A., E.D. McArthur, J.S. Haley, and D.K. Mann, comps. Proceedings: Wildland shrub and arid land restoration symposium October 19-21, 1993. Las Vagas, NV. Gen. Technical Report INT-GTR-315, Ogden ,UT, U.S. Department of Agriculture, Forest Service, Intermountain Research Station.

Linhart, Y.B. and M.C. Grant. 1996. Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology and Systematics 27:237–277.

Luikart, G., W.B. Sherwin, B.M. Steele, and F.W. Allendorf. 1998. Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Molecular Ecology 7:963–974.

McKay, J.K. and R.G. Latta. 2002. Adaptive population divergence: markers, QTL and traits. Trends in Ecology and Evolution 17:285–291.

Nagy, E.S. and K.J. Rice. 1997. Local adaptation in two subspecies of an annual plant: Implications for migration and gene flow. Evolution 51:1079–1089.

Purvis, A. and A. Hector. 2000. Getting the measure of biodiversity. Nature 405:212–219.

Reed, D.H. and R. Frankham. 2001. How closely correlated are molecular and quantitative measures of genetic variation? A meta-analysis. Evolution 55:1095–1103.

Reed, D.H. and R. Frankham. 2003. Correlation between fitness and genetic diversity. Conservation Biology 17:230–237.

Rice, K.J. and N.C. Emery. 2003. Managing microevolution: Restoration in the face of global climate change. Frontiers in Ecology and the Environment 1:469-478.

Rice, K.J. and R.N. Mack. 1991. Ecological genetics of Bromus tectorum: I. A hierarchical analysis of phenotypic variation. Oecologia 88:77–83.

Rice, K.J. and R.N. Mack. 1991. Ecological genetics of Bromus tectorum: II. Intraspecific variation in phenotypic plasticity. Oecologia 88:84–90.

Rice, K.J. and R.N. Mack. 1991. Ecological genetics of Bromus tectorum: III. The demography of reciprocally sown populations. Oecologia 88:91–101.

Riley, S.P.D., H.B. Shaffer, S.R. Voss, and B.M. Fitzpatrick. 2003. Hybridization between a rare, native tiger salamander (Ambystoma californiense) and its introduced congener. Ecological Applications 13:1263–1275.

Rogers, D.L. 1999. Patterns of genetic variation within and between two groves of giant Sequoia (Sequoiadendron giganteum (Lindl.) Buch.): Position and age-related relationships. Report to the Pacific Southwest Research Station, USDA Forest Service, January, 1999.

Rogers, D.L. 2000. Genotypic diversity and clone size in populations of coast redwood (Sequoia sempervirens (D.Don) Endl.). Canadian Journal of Botany 78:1408–1419.

Rogers, D.L. 2004. Genetic erosion: No longer just an agricultural issue. Native Plants Journal 5:113–122.

Rogers, D.L. and A.M. Montalvo. 2004. Genetically appropriate choices for plant materials to maintain biological diversity. Online publication.

Sacks, B.N, B.R. Mitchell, C.L. Williams, and H.B. Ernest. 2005. Coyote movements and social structure along a cryptic population genetic subdivision. Molecular Ecology 14:1241–1249.

Sacks, B.N., S.K. Brown, and H.B. Ernest. 2004. Population structure of California coyotes corresponds to habitat-specific breaks and illuminates species history. Molecular Ecology 13:1265–1275.

Shaffer, H.B., G.M. Fellers, A. Magee, and S.R. Voss. 2000. The genetics of amphibian declines: Population substructure and molecular differentiation in the Yosemite toad, Bufo canorus (Anura, Bufonidae) based on single-strand conformation polymorphism analysis (SSCP) and mitochondrial DNA sequence data. Molecular Ecology 9:245–257.

Shaffer, H.B., G.M. Fellers, S.R. Voss, J.C. Oliver, and G.B. Pauly. 2004a. Species boundaries, phylogeography and conservation genetics of the red-legged frog (Rana aurora/draytonii) complex. Molecular Ecology 13:2667–2677.

Shaffer, H.B., G.B. Pauly, J.C. Oliver, and P.C. Trenham. 2004b. The molecular phylogenetics of endangerment: Cryptic variation and historical phylogeography of the California tiger salamander, Ambystoma californiense. Molecular Ecology. 13:3033–3049.

Slatkin, M. and N.H. Barton. 1989. A comparison of three indirect methods for estimating average levels of gene flow. Evolution 43:1349–1368.

Spinks, P.Q., G.B. Pauly, J.J. Crayon, and H.B. Shaffer. 2003. Survival of the western pond turtle (Emys marmorata) in an urban California environment. Biological Conservation 113:257–267.

Spinks, P.Q. and H.B. Shaffer. 2005. Range-wide molecular analysis of the western pond turtle (Emys marmorata): Cryptic variation, isolation by distance, and their conservation implications. Molecular Ecology 14:2047–2064.

Stewart, B.R., B. Fitzpatrick, Benjamin, P.C. Trenham, and H.B. Shaffer. 2004. Upland spatial distribution of sub-adult California tiger salamanders. Ecological Society of America Annual Meeting Abstracts. 89:488.

Storfer, A. 1996. Quantitative genetics: A promising approach for the assessment of genetic variation in endangered species. Trends in Ecology and Evolution 11:343–348.

Tranah, G., D.E. Campton, and B. May. 2004. Genetic evidence for hybridization of pallid and shovelnose sturgeon. Journal of Heredity 95:474–480.

Tranah, G.J., M. Bagley, J.J Agresti, and B. May. 2003. Development of codominant markers for identifying species hybrids. Conservation Genetics 4:537–541.

Trenham, P.C., W.D. Koenig, and H.B. Shaffer. 2001. Spatially autocorrelated demography and interpond dispersal in the salamander Ambystoma californiense. Ecology 82:3519–3530.

Trenham, P.C. and H.B. Shaffer. 2005. Amphibian upland habitat use and its consequences for population viability. Ecological Applications 15:1158–1168.

Workshop participants

US Fish & Wildlife Service
Harry McQuillen
Graciela Hinshaw
Valary Bloom
Diane Elam

US Geological Survey
Robert Fisher

California Department of Fish & Game
Eric Loft
Mary Ann Showers
Brenda Johnson
Betsy Bolster

California Department of Parks and Recreation
Craig Swolgaard
Roy Woodward

California Native Plant Society
Misa Ward (alternate address)
Ann Howald

UC Davis Department of Plant Sciences, CAES
Kevin Rice
Ayzik Solomeshch

UC Davis Department of Animal Science, CAES
Rachel Schwartz

UC Davis Department of Entomology, CAES
Lynn Kimsey

UC Davis Section of Evolution and Ecology, CBS
Brad Shaffer

UC Davis Wildlife and Ecology Unit, Veterinary Genetics Laboratory
Holly Ernest
Ben Sacks
Sarah Brown
Joshua Hull
Jay Well
Elizabeth Heeg

Genetic Resources Conservation Program, University of California
Deborah Rogers
Patrick McGuire


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