Multiple paternity in the Black Caiman (Melanosuchus niger) population in the Anavilhanas National Park, Brazilian Amazonia

Abstract

The formation of dominance hierarchies in which the female mates with a large dominant male is common among crocodilians. However, there is the possibility of polyandry, in which females mate with multiple partners during a single breeding season and generate offspring with multiple paternity. In the present study, eight pairs of heterologous primers developed for Alligator mississippiensis and Caiman latirostris were used to determine whether multiple paternity exists in the Black Caiman, Melanosuchus niger. For such, we analyzed 34 Black Caiman offspring from the Anavilhanas Archipelago in the Negro River (state of Amazonas, Brazil). The specimens came from six groups, each containing five or six hatchlings. Paternity exclusion and genetic identity indices were calculated to test the robustness of the microsatellite loci. Simple allele counts and maximum likelihood estimation of family clusters were used to determine the likelihood of occurrence of multiple paternity. Among the eight loci tested, five were effective at determining paternity, with paternity exclusion values close to 1.0 (QC = 0.92) and genetic identity values close to zero (IC < 0.01). Using the simple allele count, six cases of multiple paternity were detected and confirmed in three hatchling groups by four different microsatellite loci. However, maximum likelihood analysis indicated multiple paternity in all the groups analyzed, with five family clusters identified in one hatchling group alone. Considering that this species is listed according to IUCN as Lower Risk/Conservation Dependent, our results have direct conservation implications. Multiple paternity increases effective population size by maintaining genetic variation, and thus could be an important mechanism to maintain genetic diversity in isolated local populations.

Mating dynamics and multiple paternity in a long‐lived vertebrate

“…Crocodilians, which have widely varying population densities and degrees of male territoriality, provide an excellent system to explore the evolutionary and ecological drivers that underlie the observed variation in the frequency of multiple paternity (Amavet, Rosso, Markariani, & Piña, 2008;Budd, Spotila, & Mauger, 2015;Davis, Glenn, Elsey, Dessauer, & Sawyer, 2001;Lance et al, 2009;Lewis, FitzSimmons, Jamerlan, Buchan, & Grigg, 2013;Mcvay et al, 2008;Muniz et al, 2011;Ojeda, Amavet, Rueda, Siroski, & Larriera, 2017;Oliveira, Marioni, Farias, & Hrbek, 2014;Lafferriere et al, 2016;Wu & Hu, 2010). The frequency of multiple paternity observed across crocodilian taxa ranges from 32% in the Chinese alligator (Alligator sinensis) to 100% in black caiman (Melanosuchus niger) (Muniz et al, 2011;Wu & Hu, 2010).…”

“…Crocodilians, which have widely varying population densities and degrees of male territoriality, provide an excellent system to explore the evolutionary and ecological drivers that underlie the observed variation in the frequency of multiple paternity (Amavet, Rosso, Markariani, & Piña, 2008;Budd, Spotila, & Mauger, 2015;Davis, Glenn, Elsey, Dessauer, & Sawyer, 2001;Lance et al, 2009;Lewis, FitzSimmons, Jamerlan, Buchan, & Grigg, 2013;Mcvay et al, 2008;Muniz et al, 2011;Ojeda, Amavet, Rueda, Siroski, & Larriera, 2017;Oliveira, Marioni, Farias, & Hrbek, 2014;Lafferriere et al, 2016;Wu & Hu, 2010). The frequency of multiple paternity observed across crocodilian taxa ranges from 32% in the Chinese alligator (Alligator sinensis) to 100% in black caiman (Melanosuchus niger) (Muniz et al, 2011;Wu & Hu, 2010). Among crocodilians, it is not clear if the frequency of multiple paternity is driven by population density and/or mate encounter rate (Amavet et al, 2008;Budd et al, 2015;Davis et al, 2001;Lance et al, 2009;Lewis et al, 2013;McVay et al, 2008;Muniz et al, 2011;Oliveira et al, 2014;Lafferriere et al, 2016;Wu & Hu, 2010) though both have been suggested (Budd et al, 2015;Lafferriere et al, 2016).…”

“…The frequency of multiple paternity observed across crocodilian taxa ranges from 32% in the Chinese alligator (Alligator sinensis) to 100% in black caiman (Melanosuchus niger) (Muniz et al, 2011;Wu & Hu, 2010). Among crocodilians, it is not clear if the frequency of multiple paternity is driven by population density and/or mate encounter rate (Amavet et al, 2008;Budd et al, 2015;Davis et al, 2001;Lance et al, 2009;Lewis et al, 2013;McVay et al, 2008;Muniz et al, 2011;Oliveira et al, 2014;Lafferriere et al, 2016;Wu & Hu, 2010) though both have been suggested (Budd et al, 2015;Lafferriere et al, 2016).…”

Science and conservation of Amazonian crocodilians: a historical review

“…Polyandry might be beneficial to females as it increases the genetic variability of their offspring (Yasui, 1998). Multiple paternity has been detected in both species subjected to heavy hunting in the Amazon basin (Muniz et al, 2011;Oliveira, Farias, Marioni, Campos, & Hrbek, 2010;Oliveira, Marioni, Farias, & Hrbek, 2014).…”

“…Another of the mechanisms that facilitates the resilience of crocodilian populations to overhunting might be found in their mating system. Multiple paternity increases effective population size by maintaining genetic variation, and therefore acting as an important mechanism to preserve genetic diversity in isolated local populations (Chesser & Baker, 1996;Muniz et al, 2011;Rafajlovi c et al, 2013).…”