Brood mixing and reduced polyandry in a maternally mouthbrooding cichlid with elevated among‐breeder relatedness

Uniparental maternal brood care often coincides with multiple paternity and single maternity of broods, possibly reflecting benefits of polyandry and costs of uniparental care. Genetic data from the maternally mouthbrooding cichlid fish Simochromis pleurospilus revealed the opposite pattern – low polyandry and allomaternal care. More than 70% of the investigated females had mated with a single male, and 14% of the females had unrelated fry in their broods. Broods with foreign fry were in the late stage of brood care, in which females guard free‐swimming fry and recall the broods into their mouths for protection. With one exception, fostering females were related to their adopted fry at the level of first cousins (RQG > 0.12), but relatedness between fosters and adopted fry was not significantly higher than between fosters and fry tended by other females. Relatedness among breeders extended to the level of first‐order relatives. Mean relatedness among contemporaneously breeding dams (RQG = 0.08) was significantly higher than among dams breeding in different seasons (RQG = −0.04), which suggests a temporal or spatial concentration of mouthbrooding relatives. Indeed, females sometimes brood in small groups. This behaviour may reduce brood predation but will increase the risk of brood mixing, which is possibly mitigated by low costs of brood care and indirect benefits accrued by relatedness among the breeders in the group. Remarkably, the apparent inbreeding potential did not give rise to bet‐hedging polyandry or active avoidance of relatives, as half of the mated individuals were related at RQG > 0.13 and polyandry did not coincide with high within‐pair relatedness.

[1]  R Higuchi,et al.  Chelex 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. , 2013, BioTechniques.

[2]  O. Krüger Brood parasitism selects for no defence in a cuckoo host , 2011, Proceedings of the Royal Society B: Biological Sciences.

[3]  M. Taborsky,et al.  Female mouthbrooders in control of pre- and postmating sexual selection , 2011 .

[4]  M. Milinkovitch,et al.  Alien eggs in duck nests: brood parasitism or a help from Grandma? , 2011, Molecular ecology.

[5]  S. Coleman,et al.  Patterns of multiple paternity and maternity in fishes , 2011 .

[6]  K. M. Sefc Mating and Parental Care in Lake Tanganyika's Cichlids , 2011, International journal of evolutionary biology.

[7]  B. Taborsky,et al.  Resource defence or exploded lek? - A question of perspective , 2010 .

[8]  O. Jones,et al.  COLONY: a program for parentage and sibship inference from multilocus genotype data , 2010, Molecular ecology resources.

[9]  R. Alatalo,et al.  Female‐biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix) , 2010, Molecular ecology.

[10]  B. Hatchwell Cryptic Kin Selection: Kin Structure in Vertebrate Populations and Opportunities for Kin‐Directed Cooperation , 2010 .

[11]  M. Andersson,et al.  Colony kin structure and host‐parasite relatedness in the barnacle goose , 2009, Molecular ecology.

[12]  D. Ardia,et al.  Breeding synchrony through social stimulation in a spatially segregated population of European starlings , 2009, Animal Behaviour.

[13]  K. M. Sefc,et al.  Mating system variability in a mouthbrooding cichlid fish from a tropical lake , 2009, Molecular ecology.

[14]  R. O’Hara,et al.  Relatedness and spatial proximity as determinants of host–parasite interactions in the brood parasitic Barrow's goldeneye (Bucephala islandica) , 2009, Molecular ecology.

[15]  K. M. Sefc,et al.  Assessing parent numbers from offspring genotypes: the importance of marker polymorphism. , 2009, The Journal of heredity.

[16]  S. Kalinowski,et al.  Sex‐biased natal dispersal and inbreeding avoidance in American black bears as revealed by spatial genetic analyses , 2008, Molecular ecology.

[17]  B. Lyon,et al.  Conspecific Brood Parasitism in Birds: A Life-History Perspective , 2008 .

[18]  D. Gower,et al.  Care and parentage in a skin-feeding caecilian amphibian. , 2008, Journal of experimental zoology. Part A, Ecological genetics and physiology.

[19]  K. M. Sefc,et al.  High frequency of multiple paternity in broods of a socially monogamous cichlid fish with biparental nest defence , 2008, Molecular ecology.

[20]  M. Nishida,et al.  PERMANENT GENETIC RESOURCES: Isolation and characterization of microsatellite loci in the cichlid fish in Lake Victoria, Haplochromis chilotes , 2008, Molecular ecology resources.

[21]  T. Glenn,et al.  Isolation and characterization of tetranucleotide microsatellite markers in a mouth-brooding haplochromine cichlid fish (Pseudocrenilabrus multicolor victoriae) from Uganda , 2007 .

[22]  M. Reichard,et al.  Sneaking from a female perspective , 2007, Animal Behaviour.

[23]  J. Poole,et al.  Behavioural inbreeding avoidance in wild African elephants , 2007, Molecular ecology.

[24]  R. Alatalo,et al.  Restrictive mating by females on black grouse leks , 2007, Molecular ecology.

[25]  M. Andersson,et al.  Host–parasite kinship in a female‐philopatric bird population: evidence from relatedness trend analysis , 2007, Molecular ecology.

[26]  R. Wayne,et al.  Inbreeding is reduced by female-biased dispersal and mating behavior in Ethiopian wolves , 2007 .

[27]  R. Jaeger,et al.  Multiple paternity in a salamander with socially monogamous behaviour , 2006, Molecular ecology.

[28]  K. M. Sefc,et al.  Monogamy in the maternally mouthbrooding Lake Tanganyika cichlid fish Tropheus moorii , 2006, Proceedings of the Royal Society B: Biological Sciences.

[29]  B. Taborsky Mothers determine offspring size in response to own juvenile growth conditions , 2006, Biology Letters.

[30]  Aaron P. Wagner,et al.  ml‐relate: a computer program for maximum likelihood estimation of relatedness and relationship , 2006 .

[31]  B. Taborsky,et al.  The influence of juvenile and adult environments on life-history trajectories , 2006, Proceedings of the Royal Society B: Biological Sciences.

[32]  T. Glenn,et al.  Sixty polymorphic microsatellite markers for the oldfield mouse developed in Peromyscus polionotus and Peromyscus maniculatus , 2006 .

[33]  M. Webster,et al.  Paternity and paternal effort in the pumpkinseed sunfish , 2005 .

[34]  A. Jones gerud 2.0: a computer program for the reconstruction of parental genotypes from half‐sib progeny arrays with known or unknown parents , 2005 .

[35]  H. Ochi,et al.  Farming-out of offspring is a predominantly male tactics in a biparental mouthbrooding cichlid Perrisodus mircolepis , 2005, Environmental Biology of Fishes.

[36]  S. Schneider,et al.  Arlequin (version 3.0): An integrated software package for population genetics data analysis , 2005, Evolutionary bioinformatics online.

[37]  Martin I. Taylor,et al.  Evidence for genetic monogamy and female‐biased dispersal in the biparental mouthbrooding cichlid Eretmodus cyanostictus from Lake Tanganyika , 2003, Molecular ecology.

[38]  D. Wake,et al.  Directional selection has shaped the oral jaws of Lake Malawi cichlid fishes , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[39]  B. Neff Decisions about parental care in response to perceived paternity , 2003, Nature.

[40]  Martin I. Taylor,et al.  Characterization of tetranucleotide microsatellite loci in a Lake Victorian, haplochromine cichlid fish: a Pundamilia pundamilia 〈 Pundamilia nyererei hybrid , 2002 .

[41]  H. Kokko,et al.  The role of kin recognition in the evolution of conspecific brood parasitism , 2002, Animal Behaviour.

[42]  J. Streelman,et al.  Rapid isolation of CA microsatellites from the tilapia genome. , 2002, Animal genetics.

[43]  I. Owens,et al.  Evolutionary Ecology of Birds: Life Histories, Mating Systems and Extinction , 2002 .

[44]  T. Tregenza,et al.  Polyandrous females avoid costs of inbreeding , 2002, Nature.

[45]  M. Andersson,et al.  Host-parasite relatedness shown by protein fingerprinting in a brood parasitic bird. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[46]  Andrew G. Zink The Evolution of Intraspecific Brood Parasitism in Birds and Insects , 2000, The American Naturalist.

[47]  Markus Schuelke,et al.  An economic method for the fluorescent labeling of PCR fragments , 2000, Nature Biotechnology.

[48]  D. Queller,et al.  Computer software for performing likelihood tests of pedigree relationship using genetic markers , 1999, Molecular ecology.

[49]  B. Wisenden Alloparental care in fishes , 1999, Reviews in Fish Biology and Fisheries.

[50]  T. Kocher,et al.  Microsatellites DNA markers for genetics mapping in Oreochromis niloticus , 1996 .

[51]  I. Kornfield,et al.  Polygynandry inPseudotropheus zebra, a cichlid fish from Lake Malawi , 1996, Environmental Biology of Fishes.

[52]  A. Pusey,et al.  Inbreeding avoidance in animals. , 1996, Trends in ecology & evolution.

[53]  T. Burke,et al.  Intraspecific brood parasitism in the moorhen: parentage and parasite-host relationships determined by DNA fingerprinting , 1996, Behavioral Ecology and Sociobiology.

[54]  H. Ochi,et al.  Intraspecific brood-mixing of the cichlid fishPerissodus microlepis in Lake Tanganyika , 1995, Environmental Biology of Fishes.

[55]  J. R. Stauffer,et al.  Microsatellite variation demonstrates multiple paternity in lekking cichlid fishes from Lake Malawi, Africa , 1995, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[56]  R. Wootton,et al.  The costs of parental care in teleost fishes , 1995, Reviews in Fish Biology and Fisheries.

[57]  D. Westneat Nesting Synchrony by Female Red‐Winged Blackbirds: Effects on Predation and Breeding Success , 1992 .

[58]  M. Sorenson Comment: Why is conspecific nest parasitism more frequent in waterfowl than in other birds? , 1992 .

[59]  T. Nudds,et al.  Pre-hatch and post-hatch brood amalgamation in North American Anatidae: a review of hypotheses , 1988 .

[60]  W. Mrowka Brood adoption in a mouthbrooding cichlid fish: Experiments and a hypothesis , 1987, Animal Behaviour.

[61]  H. Ochi Breeding synchrony and spawning intervals in the temperate damselfishChromis notata , 1986, Environmental Biology of Fishes.

[62]  A. Fostier,et al.  Endocrine changes associated with spawning behavior and social stimuli in a wild population of rainbow trout (Salmo gairdneri). II. Females. , 1986, General and comparative endocrinology.

[63]  G. McCracken,et al.  ON ESTIMATING RELATEDNESS USING GENETIC MARKERS , 1985, Evolution; international journal of organic evolution.

[64]  D. Lewis Mixed Species Broods in Lake Malawi Cichlids: An Alternative to the Cuckoo Theory , 1980 .

[65]  K. McKaye,et al.  COMMUNAL CARE AND KIDNAPPING OF YOUNG BY PARENTAL CICHLIDS , 1977, Evolution; international journal of organic evolution.

[66]  A. Ribbink,et al.  Cuckoo among Lake Malawi cichlid fish , 1977, Nature.

[67]  M. Keenleyside The behaviour of Abudefduf zonatus (Pisces, pomacentridae) at Heron Island, Great Barrier Reef , 1972 .

[68]  H. Southern Predators and Anti-predator Behaviour of the Black-headed Gull , by Hans Kruuk. E. J. Brill, Leiden, 36 guilders. , 1965, Oryx.

[69]  H. Kruuk,et al.  Predators and anti-predator behaviour of the black-headed gull (Larus ridibundus L.) , 1964 .

[70]  G. Baerends,et al.  An introduction to the study of the ethology of cichlid fishes , 1952 .

[71]  B. Taborsky,et al.  Life-stage specific environments in a cichlid fish: implications for inducible maternal effects , 2011, Evolutionary Ecology.

[72]  S. Alonzo,et al.  Alloparental care increases mating success , 2011 .

[73]  M. Andersson,et al.  Spatial relatedness and brood parasitism in a female-philopatric bird population , 2008 .

[74]  D. Tallamy Egg dumping in insects. , 2005, Annual review of entomology.

[75]  J. Avise,et al.  Genetic mating systems and reproductive natural histories of fishes: lessons for ecology and evolution. , 2002, Annual review of genetics.

[76]  J. R. Stauffer,et al.  Intraspecific brood mixing and reduced polyandry in a maternal mouth-brooding cichlid , 1998 .

[77]  M. Taborsky Sneakers, Satellites, and Helpers: Parasitic and Cooperative Behavior in Fish Reproduction , 1994 .

[78]  桑村 哲生 Biparental mouthbrooding and guarding in a Tanganyikan cichlid Haplotaxodon microlepis. , 1988 .

[79]  柳澤 康信 Parental care in a monogamous mouthbrooding cichlid Xenotilapia flavipinnis in Lake Tanganyika. , 1986 .

[80]  B. J. Sharp,et al.  Parental behaviour and mixed broods among cichlid fish of Lake Malawi , 1980 .

[81]  A. Adriaanse Ammophila Campestris Latr. Und Ammophila Adriaansei Wilcke Ein Beitrag Zur Vergleichenden Verhaltensforschung , 1948 .