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227 2005 10 Article-Web 213..22 UC Irvine UC Irvine Previously Published Works Title Cuckoldry rates in the Molly Miller (Scartella cristata; Blenniidae), a hole-nesting marine fish with alternative reproductive tactics Permalink https://escholarship.org/uc/item/664117k2 Journal Marine Biology, 148(1) ISSN 0025-3162 Authors Mackiewicz, M Porter, BA Dakin, EE et al. Publication Date 2005 DOI 10.1007/s00227-005-0010-9 License https://creativecommons.org/licenses/by/4.0/ 4.0 Peer reviewed eScholarship.org Powered by the California Digital Library University of California Marine Biology (2005) 148: 213–221 DOI 10.1007/s00227-005-0010-9 RESEARCH ARTICLE Mark Mackiewicz Æ Brady A. Porter Elizabeth E. Dakin Æ John C. Avise Cuckoldry rates in the Molly Miller (Scartella cristata; Blenniidae), a hole-nesting marine fish with alternative reproductive tactics Received: 17 May 2004 / Accepted: 4 April 2005 / Published online: 19 August 2005 Ó Springer-Verlag 2005 Abstract Microsatellite markers were developed and Introduction employed to assess genetic maternity and paternity of embryos in nest-tended clutches of the Molly Miller In fish species with external fertilization and extended (Scartella cristata), a marine fish in which alternative parental care of offspring in nests (usually by males), reproductive tactics (ARTs) by males were recently de- intense competition for access to mates and fertilizations scribed from behavioral and morphological evidence. has frequently led to the evolution of male alternative Genetic data gathered for 1,536 surveyed progeny, from reproductive tactics (ARTs) (Gross 1991, 1996; Tabor- 23 barnacle-nest holes in a single Floridian population, sky 1994, 2001). Such ARTs, as behaviorally defined, are indicate that on average about 5.5 females (range 3–9) often associated with distinctive morphological features contributed to the pool of progeny within a nest. With of the fish as well (Gross 1982; Gross and Charnov 1980; regard to paternity, the microsatellite data demonstrate Gross and Shine 1981; Taborsky 1997). Probably the that most of the surveyed nests (82.6%) contained at most common dichotomy is between bourgeois males least some embryos that had not been sired by the nest- (nest tenders) and parasitic sneakers (Taborsky 1998). tending (bourgeois) male, and overall that 12.4% of Bourgeois males typically are large, display colorful offspring in the population had been sired via ‘‘stolen’’ secondary sexual characters, actively court females, and fertilizations by other males. These are among the tend nests (e.g., fan eggs and defend against predators). highest values of cuckoldry documented to date in nest- Sneaker males can be much smaller and less colorful, tending fishes, and they support and quantify the notion show no proclivity to tend nests, and often have much that the nest-parasitic ART is reproductively quite suc- higher testis size relative to body mass (apparently an cessful in this species despite what would otherwise seem adaptation for sperm competition associated with nest to be highly defensible nesting sites (the restricted inte- parasitism; Taborsky 1998). Whenever a parasitic male rior space of a barnacle shell). Our estimated cuckoldry ‘‘steals’’ some fraction of fertilization events from a rates in this population of the Molly Miller are com- bourgeois male, e.g., by sneaking onto his nest and pared to those previously reported for local populations releasing sperm during a spawning episode, the nest- in other nest-tending fish species, with results discussed tender then becomes a foster parent and is said to have in the context of ecological and behavioral variables that been cuckolded. may influence relative frequencies of nest parasitism. The Molly Miller (Scartella cristata; Perciformes; Blenniidae) is an abundant combtooth blenny of tem- perate and tropical regions (Robins 1986). Found near the shoreline in rocky areas, its range in the tropical western Atlantic extends from Florida, Bermuda, and Communicated by P. W. Sammarco, Chauvin the northern Gulf through the Caribbean Sea to Brazil (Gilbert 2002; Robins 1986). The Molly Miller is a hole- M. Mackiewicz (&) Æ E. E. Dakin Æ J. C. Avise dwelling species with external fertilization. Large nest- Department of Genetics, University of Georgia, Athens, GA tending (bourgeois) males, whose elongate bodies reach 30602, USA E-mail: [email protected] up to 10 cm in length, are highly territorial and also Fax: +1-706-5830359 provide extended care to the embryos in their respective Present address: B. A. Porter nests, which are usually the hollow empty shells of Department of Biological Sciences, Duquesne University, barnacles (McEachran 1998). However, a recent com- Pittsburgh, PA 15282, USA parative study of body sizes, accessory features of the 214 reproductive tract involved in sperm production and embryos lining its inner wall were preserved in a 20% handling, and testicular glands involved in pheromone DMSO/saturated NaCl solution. Care was taken to synthesis, coupled with behavioral monitoring, docu- ensure that each bourgeois male was correctly associ- mented the presence of two other distinctive male ated with his nest. An additional 29 individuals (males, reproductive morphotypes in S. cristata (Neat et al. females, and juveniles) found swimming on the rock 2003): non-reproducing satellites (medium-sized indi- surface were collected for microsatellite development viduals that remain site-attached to a hole), and sneak- and to estimate population allele frequencies at the loci ers (small vagrant males that appear morphologically analyzed. and behaviorally specialized for releasing sperm in larger From a single adult male, genomic DNA was extracted males’ nests). In other blennioid species, intrasexual from approximately 25 mg of muscle tissue using a polymorphisms of these sorts have usually (but see also DNeasy Blood and Tissue DNA Extraction Kit (Qiagen). Neat and Locatello 2002) been taken as good indicators A modified enrichment technique from Hamilton (1999) for the presence of ARTs and nest parasitism (Goncal- was used to isolate and sequence microsatellite-containing ves et al. 2003a, b; Miranda et al. 2003; Neat 2001; DNA fragments (Croshaw and Glenn 2003; Hamilton Oliveira et al. 2000, 2001a, b, 2002). et al. 1999; Hauswaldt and Glenn 2003). Briefly, genomic Although indirect evidence for nest parasitism by DNA was digested for 30 min at 37°C with RsaI (New males can emerge from morphological assessments and England Biolabs). Fragments were then ligated to double- behavioral monitoring, marker-based genetic analyses stranded SuperSNX24 linkers (forward 5¢-GTTTAGG- have made it possible to quantify actual rates and pat- CCTAGCTAGCAGAATC-3¢; reverse 5¢-GATTCTGC- terns of reproductive cuckoldry in nature. Microsatellite TAGCTAGGCCTTAAACAAAA-3¢) and hybridized to markers, in particular, have proved invaluable for a cocktail of biotinylated oligonucleotide repeat probes: detecting and quantifying reproductive behaviors in (TG)12, (AG)12, (AAG)8, (ATC)8, (AAC)8, (AAT)12, fishes, including alternative reproductive tactics and (ACT)12, (AAAC)6, (AAAG)6, (AATC)6, (AATG)6, mating systems (Avise et al. 2002; DeWoody and Avise (ACCT)6, (ACAG)6, (ACTC)6, (ACTG)6, (AAAT)8, 2001; Jones and Avise 2001). Here we develop and em- (AACT)8, (AAGT)8, (ACAT)8, (AGAT)8, (AACC)5, ploy a battery of microsatellite markers to examine ge- (AACG)5, (AAGC)5, (AAGG)5, and (ATCC)5. Hybrid- netic parentage (maternity as well as paternity) in a ized probes were captured on a magnetic block using Floridian population of S. cristata. Of particular interest magnetic streptavidin beads (Dynal). are male cuckoldry rates, which paradoxically might be Enriched DNA was recovered by precipitation and hypothesized to be either exceptionally high (because of PCR-amplified (25 ll reaction volume) under the fol- a high density of Molly Miller nests at the surveyed lo- lowing conditions: 10 mM Tris–HCl pH 9.0, 50 mM cale, and the presence of a sneaker ART in this species), KCl, 0.1% Triton X-100, 2.0 mM MgCl, 25.0% g/ml or exceptionally low (if the barnacle-hole nests are as BSA, 0.2 mM each dNTP, 0.5 lM SuperSNX24 for- physically defensible by bourgeois males as they would ward primer, and 0.5 U DNA Polymerase (Promega). appear to be at face value). The genetic findings on The PCR product was ligated into a PCR 2.1-TOPO cuckoldry rates will be interpreted in the context of vector, transformed into One Shot Top10 Chemically earlier behavioral and morphological observations for Competent Escherichia coli cells, and positive colonies this species. They will also be compared to similar mi- were screened for b-galactosidase activity using the crosatellite-based reports for local populations in other materials provided in the TOPO TA cloning kit (Invi- nest-tending species, in order to address various eco- trogen). To verify insert sizes, inserts from positive col- logical and behavioral factors that might influence rel- onies were amplified using M13 primers and TaqBead ative frequencies of nest parasitism in fishes. Hot Start Polymerase (Promega). Inserts ‡500 bp were purified using QIAquick Spin Columns (Qiagen) and sequenced with Big Dye chem- Materials and methods istry (version 1.0, Applied Biosystems) on an ABI 3700 DNA Analyzer with 50 cm capillaries. Sequences were Sample collections and microsatellite development edited using Sequence Analysis Software (Applied Bio- systems) and primers flanking microsatellite regions On 12 October 2002, a collection of Molly Millers was were developed using OligoAnalyzer 3.0 (Integrated made from a single rock surface (148·204 cm) that is DNA Technologies). For each successful primer pair part of a rock jetty facing the Gulf of Mexico in St. developed, tailed PCR was employed for fluorescent Andrews State Park, Panama Beach, Florida. By screening. In each case, one of the two primers was snorkeling, we collected bourgeois males from their modified at the 5¢ end with the tag 5¢-GGAAACAGC- barnacle-hole nests and preserved them in ethanol. TATGACCATG-3¢ (Boutin-Ganache et al. 2001; Cro- Each of 38 nest-tenders was captured by placing a shaw and Glenn 2003).
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