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Quantitative Genetic Analyses of Male Color Pattern and Female Mate Choice in a Pair of Cichlid Fishes of Lake Malawi, East Africa.

Ding B, Daugherty DW, Husemann M, Chen M, Howe AE, Danley PD - PLoS ONE (2014)

Bottom Line: Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1-2 non-additive genetic factors, and 3) F2 female mate choice is not influenced by male courting effort.These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice.Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Baylor University, One Bear Place #97388, Waco, Texas, 76798, United States of America.

ABSTRACT
The traits involved in sexual selection, such as male secondary sexual characteristics and female mate choice, often co-evolve which can promote population differentiation. However, the genetic architecture of these phenotypes can influence their evolvability and thereby affect the divergence of species. The extraordinary diversity of East African cichlid fishes is often attributed to strong sexual selection and thus this system provides an excellent model to test predictions regarding the genetic architecture of sexually selected traits that contribute to reproductive isolation. In particular, theory predicts that rapid speciation is facilitated when male sexual traits and female mating preferences are controlled by a limited number of linked genes. However, few studies have examined the genetic basis of male secondary sexual traits and female mating preferences in cichlids and none have investigated the genetic architecture of both jointly. In this study, we artificially hybridized a pair of behaviorally isolated cichlid fishes from Lake Malawi and quantified both melanistic color pattern and female mate choice. We investigated the genetic architecture of both phenotypes using quantitative genetic analyses. Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1-2 non-additive genetic factors, and 3) F2 female mate choice is not influenced by male courting effort. Furthermore, a joint analysis of color pattern and female mate choice indicates that the genes underlying these two traits are unlikely to be physically linked. These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice. Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.

No MeSH data available.


Male individuals of both species with indication where scale and fin samples were taken.Maylandia benetos is at the top panel, Maylandia zebra is at the middle panel, and scale and fin tissue samples are at the lower panel. The red box indicates the area where the scale samples for melanophore counts were taken, the green box indicates where the melanophores in fins were counted.
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pone-0114798-g001: Male individuals of both species with indication where scale and fin samples were taken.Maylandia benetos is at the top panel, Maylandia zebra is at the middle panel, and scale and fin tissue samples are at the lower panel. The red box indicates the area where the scale samples for melanophore counts were taken, the green box indicates where the melanophores in fins were counted.

Mentions: The Baylor University Institutional Animal Care and Use Committee approved this research. The protocol number is 08–09. Lake Malawi National Park, the Malawi Fisheries Department granted our sampling permit.Maylandia zebra and Maylandia benetos are a pair of sympatric rock-dwelling cichlid species from Lake Malawi. While M. zebra is a cosmopolitan species that occurs at many locations across the lake, M. benetos only inhabits Mazinzi Reef in the southeastern arm of the lake [18]. At Mazinzi Reef, these two species coexist in sympatry but do not hybridize: in over 400 hours of observation, no interspecific courtship or intermediate hybrid individuals were observed (Danley, pers. obs.). The two study species differ primarily in their melanistic markings [28]; M. zebra has a bright blue ground color with 5–7 dark body bars, a black cheek, and dark banding on the pelvic fin, whereas M. benetos has a bright blue ground color and faint body barring and pelvic fin markings. Although territorial males of both species maintain a bright blue hue, the melanisitic markings of M. zebra become more conspicuous when the males are territorial and fade when the male is stressed (Fig. 1). In contrast the melanistic markings of M. benetos become faint when territorial and their melanistic markings only become apparent when stressed. Females and subdominant males of both species are drab brown (M. zebra) or drab olive (M. benetos). Female M. zebra display similar melanisitic markings as observed in male M. zebra; however, the markings are much less conspicuous than those of the territorial M. zebra males [28]. A previous study of this species pair found that visual cues alone are sufficient for conspecific mate recognition and that melanistic patterning may play a significant role in the reproductive isolation of these species [28]. The mating behaviors of the two species are nearly identical [50] and involve elements such as quiver, lateral display and circling. Both species mate year round, are maternal mouthbrooders, and have a reproductive cycle that varies from 28 to 30 days at 28°C under laboratory conditions (Ding, pers. obs.).


Quantitative Genetic Analyses of Male Color Pattern and Female Mate Choice in a Pair of Cichlid Fishes of Lake Malawi, East Africa.

Ding B, Daugherty DW, Husemann M, Chen M, Howe AE, Danley PD - PLoS ONE (2014)

Male individuals of both species with indication where scale and fin samples were taken.Maylandia benetos is at the top panel, Maylandia zebra is at the middle panel, and scale and fin tissue samples are at the lower panel. The red box indicates the area where the scale samples for melanophore counts were taken, the green box indicates where the melanophores in fins were counted.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4262453&req=5

pone-0114798-g001: Male individuals of both species with indication where scale and fin samples were taken.Maylandia benetos is at the top panel, Maylandia zebra is at the middle panel, and scale and fin tissue samples are at the lower panel. The red box indicates the area where the scale samples for melanophore counts were taken, the green box indicates where the melanophores in fins were counted.
Mentions: The Baylor University Institutional Animal Care and Use Committee approved this research. The protocol number is 08–09. Lake Malawi National Park, the Malawi Fisheries Department granted our sampling permit.Maylandia zebra and Maylandia benetos are a pair of sympatric rock-dwelling cichlid species from Lake Malawi. While M. zebra is a cosmopolitan species that occurs at many locations across the lake, M. benetos only inhabits Mazinzi Reef in the southeastern arm of the lake [18]. At Mazinzi Reef, these two species coexist in sympatry but do not hybridize: in over 400 hours of observation, no interspecific courtship or intermediate hybrid individuals were observed (Danley, pers. obs.). The two study species differ primarily in their melanistic markings [28]; M. zebra has a bright blue ground color with 5–7 dark body bars, a black cheek, and dark banding on the pelvic fin, whereas M. benetos has a bright blue ground color and faint body barring and pelvic fin markings. Although territorial males of both species maintain a bright blue hue, the melanisitic markings of M. zebra become more conspicuous when the males are territorial and fade when the male is stressed (Fig. 1). In contrast the melanistic markings of M. benetos become faint when territorial and their melanistic markings only become apparent when stressed. Females and subdominant males of both species are drab brown (M. zebra) or drab olive (M. benetos). Female M. zebra display similar melanisitic markings as observed in male M. zebra; however, the markings are much less conspicuous than those of the territorial M. zebra males [28]. A previous study of this species pair found that visual cues alone are sufficient for conspecific mate recognition and that melanistic patterning may play a significant role in the reproductive isolation of these species [28]. The mating behaviors of the two species are nearly identical [50] and involve elements such as quiver, lateral display and circling. Both species mate year round, are maternal mouthbrooders, and have a reproductive cycle that varies from 28 to 30 days at 28°C under laboratory conditions (Ding, pers. obs.).

Bottom Line: Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1-2 non-additive genetic factors, and 3) F2 female mate choice is not influenced by male courting effort.These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice.Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.

View Article: PubMed Central - PubMed

Affiliation: Biology Department, Baylor University, One Bear Place #97388, Waco, Texas, 76798, United States of America.

ABSTRACT
The traits involved in sexual selection, such as male secondary sexual characteristics and female mate choice, often co-evolve which can promote population differentiation. However, the genetic architecture of these phenotypes can influence their evolvability and thereby affect the divergence of species. The extraordinary diversity of East African cichlid fishes is often attributed to strong sexual selection and thus this system provides an excellent model to test predictions regarding the genetic architecture of sexually selected traits that contribute to reproductive isolation. In particular, theory predicts that rapid speciation is facilitated when male sexual traits and female mating preferences are controlled by a limited number of linked genes. However, few studies have examined the genetic basis of male secondary sexual traits and female mating preferences in cichlids and none have investigated the genetic architecture of both jointly. In this study, we artificially hybridized a pair of behaviorally isolated cichlid fishes from Lake Malawi and quantified both melanistic color pattern and female mate choice. We investigated the genetic architecture of both phenotypes using quantitative genetic analyses. Our results suggest that 1) many non-additively acting genetic factors influence melanistic color patterns, 2) female mate choice may be controlled by a minimum of 1-2 non-additive genetic factors, and 3) F2 female mate choice is not influenced by male courting effort. Furthermore, a joint analysis of color pattern and female mate choice indicates that the genes underlying these two traits are unlikely to be physically linked. These results suggest that reproductive isolation may evolve rapidly owing to the few genetic factors underlying female mate choice. Hence, female mate choice likely played an important role in the unparalleled speciation of East African cichlid fish.

No MeSH data available.