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Observations of Social Polygyny, Allonursing, Extrapair Copulation, and Inbreeding in Urban San Joaquin Kit Foxes (Vulpes Macrotis Mutica)

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Observations of Social Polygyny, Allonursing, Extrapair Copulation, and Inbreeding in Urban San Joaquin Kit Foxes (Vulpes Macrotis Mutica) OBSERVATIONS OF SOCIAL POLYGYNY, ALLONURSING, EXTRAPAIR COPULATION, AND INBREEDING IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA) Authors: Tory L. Westall, Brian L. Cypher, Katherine Ralls, and Tammy Wilbert Source: The Southwestern Naturalist, 63(4) : 271-276 Published By: Southwestern Association of Naturalists URL: https://doi.org/10.1894/0038-4909-63-4-271 BioOne Complete (complete.BioOne.org) is a full-text database of 200 subscribed and open-access titles in the biological, ecological, and environmental sciences published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Complete website, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/terms-o-use. Usage of BioOne Complete content is strictly limited to personal, educational, and non - commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Downloaded From: https://bioone.org/journals/The-Southwestern-Naturalist on 28 Oct 2019 Terms of Use: https://bioone.org/terms-of-use Access provided by Southwestern Association of Naturalists December 2018 Notes 271 THE SOUTHWESTERN NATURALIST 63(4): 271–276 OBSERVATIONS OF SOCIAL POLYGYNY, ALLONURSING, EXTRAPAIR COPULATION, AND INBREEDING IN URBAN SAN JOAQUIN KIT FOXES (VULPES MACROTIS MUTICA) TORY L. WESTALL,* BRIAN L. CYPHER,KATHERINE RALLS, AND TAMMY WILBERT Endangered Species Recovery Program, California State University, Stanislaus, Turlock, CA 95382 (TLW, BLC) Smithsonian Conservation Biology Institute, Washington, DC 20008 (KR, TW) *Correspondent: [email protected] ABSTRACT—San Joaquin kit foxes (Vulpes macrotis mutica) are typically socially monogamous. During the 2012 breeding season in Bakersfield, California, where food is abundant, population density is high, and dispersal potential is low, we documented two cases of social polygyny. Both groups had two litters; we documented allonursing in one group. In both groups the two mothers were not closely related and the ‘‘helper’’ was not closely related to the other adults. All four reproducing females had at least one pup sired by an extragroup male. One female had three inbred pups that resulted from matings with first-degree relatives. The unique conditions associated with the urban environment may alter kit fox social ecology. RESUMEN—El comportamiento social de los zorros de San Joaqu´ın (Vulpes macrotis mutica)est´ıpicamente mon´ogamo. Durante la temporada de reproducci´on de 2012 en Bakersfield, California, donde la comida es abundante, la densidad poblacional es alta y el potencial de dispersi´on bajo, documentamos dos casos de poliginia social. Ambos grupos tuvieron dos camadas; documentamos crianza cooperativa en un grupo. En ambos grupos, las dos madres no estuvieron estrechamente relacionadas entre s´ıyla‘‘cooperante’’ no estuvo estrechamente relacionada con los dem´as adultos. Las cuatro hembras reproductoras tuvieron al menos un cachorro engendrado por un macho externo al grupo. Una hembra tuvo tres cr´ıas consangu´ıneas provenientes de apareamientos con parientes de primer grado. Las particulares condiciones asociadas al entorno urbano pueden alterar la ecolog´ıa social de los zorros de San Joaqu´ın. Monogamous mating systems are rare in mammals as a Canids are unusual among mammals because most whole but relatively common in some groups, such as species are monogamous and paternal care is also primates and canids (Kleiman, 1977). When advances in common (Kleiman, 1977; Malcolm, 1985; Asa and molecular genetics enabled wide-spread paternity test- Valdespino, 1998). Although small foxes are typically ing, monogamy was further classified as social monog- socially monogamous, they can form polygynous trios or amy (breeding adults live together in pairs) or genetic more complex social groups when resources are abun- monogamy (paired adults breed exclusively with each dant (Zabel and Taggart, 1989; Lemons et al., 2003; other; Gowaty, 1996). It is thought that social monogamy Kamler et al., 2004). Genetic testing has revealed that evolved, in most cases, from an ancestral condition in extrapair copulations are common in some species of which females were solitary and widely spaced due to foxes (Baker et al., 2004; Kitchen et al., 2006; Cameron et scarce resources (Lukas and Clutton-Brock, 2013), al., 2011). Extrapair copulations may occur more fre- although there are exceptions (Kappeler, 2014). Males quently when resources are more abundant and popula- help with care of the offspring in some socially tion densities are high (Cameron et al., 2011). monogamous species but not in others, and phyloge- The San Joaquin kit fox (Vulpes macrotis mutica)isa netic reconstructions suggest that monogamy evolved small desert-adapted canid endemic to the San Joaquin moreoftenintheabsencethanthepresenceofpaternal Desert in California (Morrell, 1972; Germano et al., care, indicating that paternal care is usually a conse- 2011). These foxes have one litter per year in the early quence rather than a cause of social monogamy (Lukas spring. They are typically socially monogamous and a and Clutton-Brock, 2013). However, paternal care has social group usually consists of a breeding pair and their been proposed as a driving force in the evolution of current offspring, although occasionally one or more monogamy in red foxes (Vulpes vulpes; Baker and Harris, pups will delay dispersal and remain in the natal home 2004). range during the next breeding season (Ralls et al., 2001, Downloaded From: https://bioone.org/journals/The-Southwestern-Naturalist on 28 Oct 2019 Terms of Use: https://bioone.org/terms-of-use Access provided by Southwestern Association of Naturalists 272 The Southwestern Naturalist vol. 63, no. 4 2007). As a result of habitat loss, the San Joaquin kit fox Hilden, Germany). We genotyped each sample at 11 has been federally listed as endangered and listed by tetranucleotide microsatellite loci (FH2137, FH2140, California as threatened (United States Fish and Wildife FH2226, FH2535, FH2561, Pez19, AHTh171, FH2054, Service, 1998). As a result of agricultural, industrial, and FH2328, FH2848, and Ren162) that had previously been urban development, the San Joaquin kit fox exists in a proven to be reliable for kit fox (Smith et al., 2006). For meta-population consisting of several small satellite each DNA extract, we performed two to three polymerase populations and three core areas (Cypher et al., 2013). chain reaction replicates of each microsatellite to ensure In addition, a fourth substantial population has adapted reproducible genotypes, with two replicates for heterozy- to living in the urban environment in Bakersfield, gous loci and three replicates for homozygous loci. We California (Cypher and Frost, 1999; Cypher, 2010). used fluorescently labeled forward primers (TET, HEX, or In Bakersfield, it is more common for kit fox social FAM) to visualize the products on an ABI PRISM 3130 groups to have an extra adult, likely because of the Genetic Analyzer (Applied Biosystems, Foster City, Cal- abundance of anthropogenic food (Cypher and Frost, ifornia). We scored the size of each fragment using 1999; Newsome et al., 2010). These are thought to be Genemappert (Thermo Fisher Scientific, Waltham, Mas- mainly pups from the previous year and are termed sachusetts) software. Every microsatellite was genotyped ‘‘helpers’’ (Macdonald, 1979; Ralls et al., 2001). Field with a positive and negative control to eliminate any observations have been conducted on the Bakersfield kit contamination and to standardize allele sizes across all foxes since 1997. In 2012, while conducting a larger study data. on parental care (Westall, 2015), we observed two social We compared the genotypes of individuals in our two groups that each had one male, two adult females, a groups with 342 individuals captured in Bakersfield from helper, and two litters. We documented the behavior of 2000 to 2011 that had already been genotyped at the same these groups through direct observations and determined loci (unpubl. data). The larger data set did have Hardy- the genetic relationships among individuals using 11 Weinberg disequilibrium and linkage disequilibrium, but microsatellite markers. this is expected given that the samples include family We trapped foxes in early January 2012 to gather groups. In addition, the individuals are only sampled relevant biological information and samples. We captured from certain areas of Bakersfield and not the entire foxes with wire-mesh box traps (38 · 38 · 107 cm) that population of kit foxes, which is likely to produce Hardy- were baited with cat food, hot dogs, and sardines. For the Weinberg disequilibrium and linkage disequilibrium. animals’ protection, we placed traps in secure locations However, we do not believe these issues are large enough away from well-trafficked areas and covered the traps with to affect parentage of assignment. oiled cloth tarps to guard against the elements. We We estimated the coefficient of relationship (r) examined each fox to determine age, sex, and reproduc- between individuals within each social group using the tive condition and applied a uniquely numbered ear-tag Queller-Goodnight
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