The role of natural selection in human evolution – insights from Latin America

Salzano, Francisco M.

doi:10.1590/1678-4685-GMB-2016-0020

Francisco M. Salzano Send correspondence to Francisco M. Salzano, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Caixa Postal 15053, 91501-970 Porto Alegre, RS, Brazil. E-mail: francisco.salzano@ufrgs.br

Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul (UFRGS), Porto Alegre, RS, Brazil

Send correspondence to Francisco M. Salzano, Departamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Caixa Postal 15053, 91501-970 Porto Alegre, RS, Brazil. E-mail: francisco.salzano@ufrgs.br

I. The descent or origin of humans
- I.1
  Proofs of descent of human from some inferior forms
- I.2
  How humans developed from some inferior forms
- I.3
  Comparison between the mental abilities of humans and of inferior animals
- I.4
  Development of the intellectual and moral faculties during the primitive and civilized ages
- I.5
  Human affinity and genealogy
- I.6
  The human races
II. Sexual selection
- II.1
  Principles of sexual selection
- II.2
  Sexual secondary characteristics in the inferior classes of the animal world
- II.3
  Sexual secondary characteristics of insects
- II.4
  Sexual secondary characteristics of fishes, amphibians, and reptiles
- II.5
  Sexual secondary characteristics of birds
- II.6
  Sexual secondary characteristics of mammals
III. Sexual selection in relation to humans and conclusion
- III.1
  Human sexual secondary characteristics
- III.2
  Conclusion

I. Molecular variation: findings and interpretation
- I.1
  Scientific hypotheses, natural selection and the neutrality theory of protein evolution, by F.J. Ayala
- I.2
  Evolutionary rates in proteins and the cost of natural selection: implications for neutral mutations, by W.M. Fitch
- I.3
  Rates of biochemical and chromosomal changes in the vertebrates, by S. Ohno
- I.4
  Enzyme polymorphisms and the neutral hypothesis of molecular evolution, by H. Harris
II. Hominid evolution
- II.1
  Long or short hominid phylogenies? Paleontological and molecular evidences, by P.V. Tobias
III. Population structure
- III.1
  Models of population structure and reality, by J.S. Friedlander
- II.2
  Kinship, fitness, and evolution, by N.E. Morton
- II.3
  Fertility differentials and their significance for human evolution, by J. Gomila
- II.4
  Frequency-dependant and density-dependent natural selection, by B. Clarke
IV. Causal factors in the distribution of quantitative and qualitative traits
- IV.1
  Natural selection and human morphology, by T. Bielicki
- IV.2
  Interpopulation variability in polymorphic systems, by F.M. Salzano
- IV.3
  Selection and the blood group polymorphisms, by T.E. Reed
- IV.4
  ABO blood groups, the HLA system and disease, by F. Vogel
- IV.5
  G6PD and abnormal hemoglobin polymorphisms – evidence regarding malarial selection, by A.G. Motulsky
V. The nature of our genetic load
- V.1
  Adaptation and genetic load, by N. Freire-Maia
- V.2
  The genetic consequences of inbreeding, by L.D. Sanghvi
- V.3
  The load due to chromosome abnormalities in man, by P.A. Jacobs
VI. The role of culture
- VI.1
  The study of "natural" selection in man: last chance, by J.V. Neel
- VI.2
  Fertility, mortality and culture: the changing pattern of natural selection, by D.F. Roberts
- VI.3
  Cultural and biological adaptation in man, by J. Huizinga
VII. An attempt at a synthesis
- VII.1
  Some key problems in the study of natural selection in man, by F.M. Salzano and all contributors

I. Methods
- I.1
  Use of the bacterial clustered regularly interspaced short palindromic repeats (CRISPR) system to serum for genes required for proliferation and survival in the near-haploid human KBM7 chronic myelogenous leukemia (CML) cell line
- I.2
  Independently, generation at random through retroviral gene-trap mutagenesis, selection for a phenotype, and monitoring by sequencing the viral integration sites to pinpoint the causal genes
- I.3
  For both methods, computation of a score for each gene that reflects the fitness cost imposed by the inactivation of the gene
- I.4
  Comparison with functional profiling experiments conducted in the yeast Saccharomyces cerevisae
- I.5
  Comparison of two CML and two Burkitt's lymphoma cell lines
II. Results
- II.1
  Of the 18,166 genes targeted by the library, 1878 (10%) scored as essential for optimal proliferation
- II.2
  Results with the second method (item I.2) provided essentially the same picture
- II.3
  Essential genes were more broadly retained across species, showed higher levels of conservation between closely related species, and contained fewer inactivating polymorphisms in humans, than their dispensable counterparts
- II.4
  Essential genes also tended to have higher expression and encoded proteins that engage in more protein-protein interactions
- II.5
  Differences in essential genes in the four cell lines studied might represent attractive targets for antineoplastic therapies

Geographical populations	No. of individuals studied	ACTN3R577X*- frequencies (%)
Africa	794	9.3
Middle East	356	39.2
Europe	445	44.3
Central and South Asia	199	50.2
East Asia	581	47.7
Oceania	35	49.5
Americas	394	76.4

Population	Mode of subsistence	No. studied	NAT2 haplotypes (%)¹ 1 The phenotype associated to *4 is rapid; for the three others, slow.
Population	Mode of subsistence	No. studied	*4	*5B	*6A	*7B	Others
Native Americans
Mesoamericans	Agriculturalists	16	35	25	0	44	6
Amazonian and Central Brazil	Hunter-gatherers	166	31	36	5	25	3
Southern	Agriculturalists	68	44	10	6	38	2
Chaco	Agriculturalists	44	77	14	0	9	0
Mestizo/Amerindian
Mexicans	Urban	68	25	10	16	46	3
Andeans	Agriculturalists	134	36	25	16	13	10
Siberians
Eskimo	Hunter-gatherers	76	26	35	25	12	2
Africa	Several	2,100	10	30	22	2	36
Europe	Several	9,848	22	40	27	2	9
Asia	Several	8,500	48	11	23	10	8

Gene	Chromosome and cluster¹ 1 Clusters 1 and 2 show indications of positive selection in the Americas; Clusters 4 and 5 positive selection in Africa; Clusters 6-7, convergent evolution in Africa and the Americas.	Biological function
SCP2	1,1	Cholesterol trafficking and metabolism
CWH43	4,3	Lipid metabolism
DCUN1D4	4,4	Muscle development
LRRC66	4,4	Muscle development
SGCB	4,4	Muscle development
SPATA1	4,4	Muscle development
C5orf34	5,5	Unknown
CLL28	5,5	Immunity to viral infections
NNT	5,5	Free-radical detoxification
HSF2	6,6	Regulation of body temperature
PKIB	6,6	Cell proliferation
SERINC1	6,6	Unknown
FKBP6	7,7	Sperm function
NSUN5	7,7	Vascular system, calcium metabolism
TRIM50	7,7	Vascular system, calcium metabolism

Genes	Potential function
MCM6, LCT	Lactase persistence
SLC45A2	Skin pigmentation
MHC region	Immunity
FADS1, FADS2	Fatty acid metabolism
TLR1, TLR6, TLR10	Immunity
ATXN2, SH2B3	Unknown
DHCR7, NADSYN1	Vitamin D metabolism
GRM5	Skin pigmentation
SLC22A4	Ergothioneine transport
ZKSCAN3, ZSCAN31	Autophagy, Lung function
Chr13 rs 1979866	Unknown
HERC2, OCA2	Eye color

The role of natural selection in human evolution – insights from Latin America

Abstract