Evidence of multiple paternity and cooperative parental care in the so called monogamous silver arowana Osteoglossum bicirrhosum (Osteoglossiformes: Osteoglossidae)

Abstract

Monogamy is rare in fishes and is usually associated with elaborate parental care. When parental care is present in fishes, it is usually the male that is responsible, and it is believed that there is a relationship between the high energetic investment and the certainty of paternity (except in the case of sneaker males). Osteoglossum bicirrhosum is considered a monogamous fish, and has particular behavioral traits that permit the study of mating systems and parental care, such as male mouthbrooding. We investigated the genetic relationships of males with the broods found in their oral cavities in Osteoglossum samples collected in a natural environment in the lower Purus river basin, Amazonas, Brazil. Fourteen broods were analyzed for parentage (268 young and 14 adult males) using eight microsatellite loci. The results indicate that eleven broods show a monogamous system. In one brood, however, approximately 50% of the young were genetically compatible with being offspring of another male, and in another two broods, none of the subsampled young were compatible with the genotypes of the brooding male. The result of this first brood may be explained by the extra-parental contribution of a sneaker male, whereas cooperative parental care may explain the result in the other two broods.Monogamia é rara em peixes e está geralmente associada a cuidado parental elaborado. Quando cuidado parental está presente em peixes, usualmente o macho é responsável, e acredita-se que exista uma relação entre investimento energético elevado e a certeza da paternidade (exceto no caso de machos oportunistas). Osteoglossum bicirrhosum é considerado monogâmico e possui determinadas características comportamentais que permitem o estudo de sistemas de acasalamento e cuidado parental, como incubação bucal dos ovos e filhotes pelos machos. Quatorze ninhadas (268 filhotes e 14 machos adultos) foram coletadas em ambiente natural na bacia do baixo rio Purus, Amazonas, Brasil e analisadas para parentesco utilizando oito loci de microssatélites. Os resultados sugeriram, para onze ninhadas, um sistema de acasalamento monogâmico. Em uma ninhada, no entanto, cerca de 50% dos jovens eram geneticamente compatíveis como sendo descendentes de outro macho, e em outras duas ninhadas nenhum dos filhotes amostrados eram filhos dos machos que estavam realizando o cuidado. O resultado da primeira ninhada pode ser explicado pela contribuição extra-par de um macho oportunista, enquanto que o cuidado parental cooperativo pode explicar os resultados nas outras duas ninhadas.

Variations in reproductive strategy of the silver Arowana, Osteoglossum bicirrhosum Cuvier, 1829 from four sub-basins of the Peruvian Amazon

“…The different breeding seasons and sedentary nature of the species should result in a reduced gene flow between sub‐basins, hence inducing genetic structuring. Although microsatellite markers are available for the silver Arowana (Silva et al., ), they have only been used to test for multiple paternity in the species (Verba et al., ) and no population genetic study has thus far been carried out. Yet, as previously pointed out (Duponchelle et al., ), the growing concerns regarding O. bicirrhosum conservation (Moreau and Coomes, , ) emphasize the need for comparative life history and genetics studies at the inter‐ and intra‐basin levels (with on‐site sampling) in order to understand the population structuring of this species and to define appropriate management strategies.…”

“…The reproductive biology of the silver Arowana is relatively well described since the early studies of Goulding (, ) and Aragao (). Recently, patterns of reproductive investment were further investigated in the Mamirauá Reserve (Queiroz, ) and the potential role of male aggregations was explored (Verba et al., ). In Peru, its reproductive characteristics were studied in one lake of the Putumayo River (Cortegano et al., ) and further information also exists in unpublished dissertations (Ayala, ; Tang and Gomez Noriega, ).…”

Interspecific Genetic Differences and Historical Demography in South American Arowanas (Osteoglossiformes, Osteoglossidae, Osteoglossum)

“…Potential climatic niche for O. bicirrhosum and O. ferreirai were estimated for both species based on occurrence data for O. bicirrhosum (3 localities from the current study; 3 localities from Verba et al [55]; 54 localities from Species Link database, ; and 89 localities from the Global Biodiversity Information Facility—GBIF, ) and O. ferreirai (one locality from the current study; six localities from Queiroz and Camargo [9]; two localities from Species Link database; and 16 localities from GBIF). Models were constructed in biomod2 [56] with combination of nine distribution algorithms, including artificial neural networks (ANN; [57]), mixture discriminant analysis (MDA; [58]), multivariate adaptive regression splines (MARS; [59]), surface range envelop (SRE; [60]), classification tree analysis (CTA; [61]), generalized linear models (GLM; [62]), generalized boosted models (GBM; [63]), random forests [64], and maximum entropy (Maxent; [65]).…”

Sperm competition, sexual selection and the diverse reproductive biology of Osteoglossiformes

“…In contrast, Osteoglossum bicirrhosum are serially monogamous and form pairs every breeding season (Queiroz, 2008), indicating low risk of multipaternity and sperm competition. Nonetheless, another osteoglossid species, Arapaima gigas , constructs nests (Lüling, 1964), a behaviour associated with low sperm competition, and also exhibits multipaternity (Verba et al ., 2014), a feature associated with high sperm competition.…”