Group composition, relatedness, and dispersal in the cooperatively breeding cichlid Neolamprologus obscurus

Abstract

Cooperative breeding has been studied intensively in many species of birds and mammals but remain less well studied in fish. We report a remarkable new example of a cooperatively breeding cichlid from Lake Tanganyika, Neolamprologus obscurus. Using field observations and microsatellite DNA analyses, we studied group structure, helping behavior, relatedness, and dispersal of this species. We present four major observations. First, large territorial breeding males mated with one to eight breeding females, each of which was territorial and unrelated to another. Second, one to ten smaller fish ("subordinates") of both sexes were allowed to stay inside the breeding females' territories. Subordinates were often highly related to both the respective breeding male and female and performed territory defense and shelter maintenance, which is regarded as helping behaviors. Third, one to three subordinate males, similar in size to breeding females, were allowed to stay inside a breeding male's territory but were not tolerated in the breeding females' territories. Pairwise relatedness suggests these individuals are usually sons of the respective breeding male. Fourth, pairwise relatedness estimates suggest that juveniles delay dispersal and assist their mothers in raising offspring. As female subordinates grow up, they leave the father's territory and disperse into other groups. In contrast, male subordinates leave their mother's territory but remain within the territory of their father. The described social system makes N. obscurus a promising new model species to study the evolution of cooperative breeding.

Within‐group relatedness is correlated with colony‐level social structure and reproductive sharing in a social fish

“…Subordinate males in a closely related species ( Neolamprologus obscurus ) seem to adopt this strategy: they disperse from the territory of their mother, but remain within the larger territory of their father (Tanaka et al . ).…”

“…), they may wait to disperse from their father's territory until they reach a size at which they may be able to challenge for a dominant breeding position in another group or can opportunistically disperse to a vacant territory (Tanaka et al . ). Subordinates in the closely related N. obscurus appear to adopt similar strategies—subordinate females disperse away from their father's territory at a smaller size, but subordinate males remain in their father's territory, likely because subordinate males are more tolerated in the territory of their father than a territory of an unrelated male (Tanaka et al .…”

Heritabilities, social environment effects and genetic correlations of social behaviours in a cooperatively breeding vertebrate

“…Comparing N. pulcher 's genetic architecture of social behaviours to those of other closely related cichlid species that differ in their degree of sociality and cooperative breeding might shed light on the evolution of sociality within this lineage. For instance, the Lamprologini tribe of Lake Tanganyika cichlids comprises around one hundred species which range from nonsocial to highly social and represent a system in which cooperative breeding has evolved repeatedly (Dey et al., ; Heg & Bachar, ; Taborsky, ; Tanaka et al., ). Furthermore, comparisons of genetic correlations between social behaviours in other cooperatively breeding animals, for instance meerkats (Huchard et al., ), red squirrels (Taylor et al., ), yellow‐bellied marmots (Petelle et al., ) but also cooperatively breeding birds (Hunter, ; Komdeur, ) and insects (Leadbeater et al., ; Queller et al., ), could also reveal whether general patterns in cooperative breeders exist, which would contribute to better understand how cooperative breeding evolves.…”

Insufficient data render comparative analyses of the evolution of cooperative breeding mere speculation: A reply to Dey et al.

“…The multi-male/multi-female category described in Heg and Bachar (2006), which has been referred to by Tanaka et al (2018), denotes groups consisting of multiple sexually mature males and females. To what extent these adult subordinates gain reproductive share is known from 6 cooperatively breeding cichlids for which genetic data are available (Neolamprologus pulcher, N. savoryi, N. obscurus, N. multifasciatus, Julidochromis ornatus, J. transcriptus;see Kohler, 1998;Awata, Munehara, & Kohda, 2005;Dierkes, Heg, Taborsky, Skubic, & Achmann, 2005;Kohda et al, 2009;Tanaka et al, 2015;Hellmann et al, 2016;Heg et al in revision; see Taborsky, 2009Taborsky, , 2016. Without exception, all these studies revealed that groups in the respective species contain larvae, young or helpers of different degrees of relatedness to the breeders, revealing that they are genetically non-monogamous.…”

“…Additionally, immigration, which occurs regularly in the cooperatively breeding cichlids investigated thus far (see Taborsky, 2016 for review), significantly reduces relatedness between helpers and beneficiaries. Consequently, in the cooperatively breeding cichlids for which genetic data are available, the mean within-group relatedness values are clearly below 0.5 (Awata et al, 2005;Dierkes et al, 2005;Kohler, 1998;Taborsky, 2009;Tanaka et al, 2015), varying with age and size of the subordinates (Dierkes et al, 2005). Dey et al (2019) state that the alternative phylogenetic trees presented in Tanaka et al (2018) also suggest 4-5 transitions to cooperative breeding.…”