Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia

Paul J. Wilson, Chris M. Wood, Patrick J. Walsh, Annie N. Bergman, Harold L. Bergman, Pierre Laurent, Bradley N. White

Research output: Contribution to journalArticle

21 Citations (Scopus)

Abstract

The Magadi tilapia (Alcolapia grahami, formerly Oreochromis alcalicus grahami) is a remarkable example of teleost life in an extreme environment. Typical conditions include water pH = 10, titration alkalinity > 300 mM, osmolality = 525 mOsm, temperatures ranging from 23° to 42°C, and O 2 levels fluctuating diurnally between extreme hyperoxia and anoxia. A number of relatively small tilapia populations are present in various thermal spring lagoons around the margin of the lake separated by kilometers of solid trona crust (floating Na2CO3) underlain by anoxic water. Despite the apparent isolation of different populations, annual floods may provide opportunities for exchange of fish across the surface of the trona and subsequent gene flow. To assess the question of isolation among Lake Magadi populations, we analyzed the variable control region of the mitochondrial DNA (mtDNA) from six lagoons. A total of seven mtDNA haplotypes, including three common haplotypes, were observed in all six populations. Several of the Lake Magadi populations showed haplotype frequencies indicative of differentiation, while others showed very little. However, differentiation among lagoon populations was discordant with their geographical distribution along the shoreline. All populations exhibited the unusual trait of 100% ureotelism but specialized morphological and physiological characteristics were observed among several of the lagoon systems. In addition, distinct differences were observed in the osmolality among the lagoons with levels as high as 1,400-1,700 mOsm kg-1, with corresponding differences in the natural levels of whole-body urea. These levels of osmotic pressure proved fatal to fish from less alkaline systems but remarkably were also fatal to the fish that inhabited lagoons with this water chemistry. Upon more detailed inspection, specific adaptations to differential conditions in the lagoon habitat were identified that allowed survival of these cichlids. Additional evidence against potential for gene flow among lagoons despite the sharing of common mtDNA haplotypes was that the osmolality of floodwaters following a heavy rain showed lethal levels exceeding 1,700 mOsm kg-1. In isolation, different mtDNA haplotypes would be predicted to go to fixation in different populations due to rapid generation times and the small effective population sizes in a number of lagoons. We propose a model of balancing selection to maintain common mtDNA sequences through a common selection pressure among lagoons that is based on microhabitats utilized by the tilapia.

Original languageEnglish
Pages (from-to)537-555
Number of pages19
JournalPhysiological and Biochemical Zoology
Volume77
Issue number4
DOIs
StatePublished - Jul 1 2004

Fingerprint

Physiological Adaptation
Tilapia
Genetic Structures
Lakes
Mitochondrial DNA
Haplotypes
Fish
haplotypes
mitochondrial DNA
Population
osmolality
Osmolar Concentration
Water
Tilapia (Cichlidae)
Fishes
Genes
Geothermal springs
Gene Flow
Geographical distribution
lakes

ASJC Scopus subject areas

  • Animal Science and Zoology
  • Physiology
  • Physiology (medical)

Cite this

Wilson, P. J., Wood, C. M., Walsh, P. J., Bergman, A. N., Bergman, H. L., Laurent, P., & White, B. N. (2004). Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia. Physiological and Biochemical Zoology, 77(4), 537-555. https://doi.org/10.1086/422054

Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia. / Wilson, Paul J.; Wood, Chris M.; Walsh, Patrick J.; Bergman, Annie N.; Bergman, Harold L.; Laurent, Pierre; White, Bradley N.

In: Physiological and Biochemical Zoology, Vol. 77, No. 4, 01.07.2004, p. 537-555.

Research output: Contribution to journalArticle

Wilson, Paul J. ; Wood, Chris M. ; Walsh, Patrick J. ; Bergman, Annie N. ; Bergman, Harold L. ; Laurent, Pierre ; White, Bradley N. / Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia. In: Physiological and Biochemical Zoology. 2004 ; Vol. 77, No. 4. pp. 537-555.
@article{24e334a3ee2f41b381462f38fac359c9,
title = "Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia",
abstract = "The Magadi tilapia (Alcolapia grahami, formerly Oreochromis alcalicus grahami) is a remarkable example of teleost life in an extreme environment. Typical conditions include water pH = 10, titration alkalinity > 300 mM, osmolality = 525 mOsm, temperatures ranging from 23° to 42°C, and O 2 levels fluctuating diurnally between extreme hyperoxia and anoxia. A number of relatively small tilapia populations are present in various thermal spring lagoons around the margin of the lake separated by kilometers of solid trona crust (floating Na2CO3) underlain by anoxic water. Despite the apparent isolation of different populations, annual floods may provide opportunities for exchange of fish across the surface of the trona and subsequent gene flow. To assess the question of isolation among Lake Magadi populations, we analyzed the variable control region of the mitochondrial DNA (mtDNA) from six lagoons. A total of seven mtDNA haplotypes, including three common haplotypes, were observed in all six populations. Several of the Lake Magadi populations showed haplotype frequencies indicative of differentiation, while others showed very little. However, differentiation among lagoon populations was discordant with their geographical distribution along the shoreline. All populations exhibited the unusual trait of 100{\%} ureotelism but specialized morphological and physiological characteristics were observed among several of the lagoon systems. In addition, distinct differences were observed in the osmolality among the lagoons with levels as high as 1,400-1,700 mOsm kg-1, with corresponding differences in the natural levels of whole-body urea. These levels of osmotic pressure proved fatal to fish from less alkaline systems but remarkably were also fatal to the fish that inhabited lagoons with this water chemistry. Upon more detailed inspection, specific adaptations to differential conditions in the lagoon habitat were identified that allowed survival of these cichlids. Additional evidence against potential for gene flow among lagoons despite the sharing of common mtDNA haplotypes was that the osmolality of floodwaters following a heavy rain showed lethal levels exceeding 1,700 mOsm kg-1. In isolation, different mtDNA haplotypes would be predicted to go to fixation in different populations due to rapid generation times and the small effective population sizes in a number of lagoons. We propose a model of balancing selection to maintain common mtDNA sequences through a common selection pressure among lagoons that is based on microhabitats utilized by the tilapia.",
author = "Wilson, {Paul J.} and Wood, {Chris M.} and Walsh, {Patrick J.} and Bergman, {Annie N.} and Bergman, {Harold L.} and Pierre Laurent and White, {Bradley N.}",
year = "2004",
month = "7",
day = "1",
doi = "10.1086/422054",
language = "English",
volume = "77",
pages = "537--555",
journal = "Physiological and Biochemical Zoology",
issn = "1522-2152",
publisher = "University of Chicago",
number = "4",

}

TY - JOUR

T1 - Discordance between genetic structure and morphological, ecological, and physiological adaptation in Lake Magadi tilapia

AU - Wilson, Paul J.

AU - Wood, Chris M.

AU - Walsh, Patrick J.

AU - Bergman, Annie N.

AU - Bergman, Harold L.

AU - Laurent, Pierre

AU - White, Bradley N.

PY - 2004/7/1

Y1 - 2004/7/1

N2 - The Magadi tilapia (Alcolapia grahami, formerly Oreochromis alcalicus grahami) is a remarkable example of teleost life in an extreme environment. Typical conditions include water pH = 10, titration alkalinity > 300 mM, osmolality = 525 mOsm, temperatures ranging from 23° to 42°C, and O 2 levels fluctuating diurnally between extreme hyperoxia and anoxia. A number of relatively small tilapia populations are present in various thermal spring lagoons around the margin of the lake separated by kilometers of solid trona crust (floating Na2CO3) underlain by anoxic water. Despite the apparent isolation of different populations, annual floods may provide opportunities for exchange of fish across the surface of the trona and subsequent gene flow. To assess the question of isolation among Lake Magadi populations, we analyzed the variable control region of the mitochondrial DNA (mtDNA) from six lagoons. A total of seven mtDNA haplotypes, including three common haplotypes, were observed in all six populations. Several of the Lake Magadi populations showed haplotype frequencies indicative of differentiation, while others showed very little. However, differentiation among lagoon populations was discordant with their geographical distribution along the shoreline. All populations exhibited the unusual trait of 100% ureotelism but specialized morphological and physiological characteristics were observed among several of the lagoon systems. In addition, distinct differences were observed in the osmolality among the lagoons with levels as high as 1,400-1,700 mOsm kg-1, with corresponding differences in the natural levels of whole-body urea. These levels of osmotic pressure proved fatal to fish from less alkaline systems but remarkably were also fatal to the fish that inhabited lagoons with this water chemistry. Upon more detailed inspection, specific adaptations to differential conditions in the lagoon habitat were identified that allowed survival of these cichlids. Additional evidence against potential for gene flow among lagoons despite the sharing of common mtDNA haplotypes was that the osmolality of floodwaters following a heavy rain showed lethal levels exceeding 1,700 mOsm kg-1. In isolation, different mtDNA haplotypes would be predicted to go to fixation in different populations due to rapid generation times and the small effective population sizes in a number of lagoons. We propose a model of balancing selection to maintain common mtDNA sequences through a common selection pressure among lagoons that is based on microhabitats utilized by the tilapia.

AB - The Magadi tilapia (Alcolapia grahami, formerly Oreochromis alcalicus grahami) is a remarkable example of teleost life in an extreme environment. Typical conditions include water pH = 10, titration alkalinity > 300 mM, osmolality = 525 mOsm, temperatures ranging from 23° to 42°C, and O 2 levels fluctuating diurnally between extreme hyperoxia and anoxia. A number of relatively small tilapia populations are present in various thermal spring lagoons around the margin of the lake separated by kilometers of solid trona crust (floating Na2CO3) underlain by anoxic water. Despite the apparent isolation of different populations, annual floods may provide opportunities for exchange of fish across the surface of the trona and subsequent gene flow. To assess the question of isolation among Lake Magadi populations, we analyzed the variable control region of the mitochondrial DNA (mtDNA) from six lagoons. A total of seven mtDNA haplotypes, including three common haplotypes, were observed in all six populations. Several of the Lake Magadi populations showed haplotype frequencies indicative of differentiation, while others showed very little. However, differentiation among lagoon populations was discordant with their geographical distribution along the shoreline. All populations exhibited the unusual trait of 100% ureotelism but specialized morphological and physiological characteristics were observed among several of the lagoon systems. In addition, distinct differences were observed in the osmolality among the lagoons with levels as high as 1,400-1,700 mOsm kg-1, with corresponding differences in the natural levels of whole-body urea. These levels of osmotic pressure proved fatal to fish from less alkaline systems but remarkably were also fatal to the fish that inhabited lagoons with this water chemistry. Upon more detailed inspection, specific adaptations to differential conditions in the lagoon habitat were identified that allowed survival of these cichlids. Additional evidence against potential for gene flow among lagoons despite the sharing of common mtDNA haplotypes was that the osmolality of floodwaters following a heavy rain showed lethal levels exceeding 1,700 mOsm kg-1. In isolation, different mtDNA haplotypes would be predicted to go to fixation in different populations due to rapid generation times and the small effective population sizes in a number of lagoons. We propose a model of balancing selection to maintain common mtDNA sequences through a common selection pressure among lagoons that is based on microhabitats utilized by the tilapia.

UR - http://www.scopus.com/inward/record.url?scp=13444270801&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=13444270801&partnerID=8YFLogxK

U2 - 10.1086/422054

DO - 10.1086/422054

M3 - Article

C2 - 15449226

AN - SCOPUS:13444270801

VL - 77

SP - 537

EP - 555

JO - Physiological and Biochemical Zoology

JF - Physiological and Biochemical Zoology

SN - 1522-2152

IS - 4

ER -