How to cite this article: Herrera-Paz EF. [Genetic isolates and inbreeding customs in three rural municipalities from Honduras]. Rev Med Inst Mex Seg Soc 2016 Jul-Aug;54(4):504-13.
Received: April 27th 2015
Accepted: September 10th 2015
Edwin Francisco Herrera-Paz
Facultad de Medicina, Universidad Católica de Honduras, Campus San Pedro y San Pablo, San Pedro Sula, Honduras
Communication with: Edwin Francisco Herrera-Paz.
Telephone: (504) 9967 2450
Background: The isonymic method has been amply used to assess the approximate genetic structure of human communities. The objective of the study was to evaluate the magnitude of genetic isolation and inbreeding customs in 57 communities from three rural municipalities of Honduras using isonymy techniques.
Methods: The list of 408 different surnames from 20712 voters registered in the national electoral organism, residing in the 57 Honduran communities, was used for this study. For each community, random (IR), non-random (IN), and total (IT) isonymy values were calculated in order to assess inbreeding coefficients FST, FIS and FIT.
Results: High consanguinity due to isolation and to endogamous customs was unveiled in many communities. Significant deviation from the exogamous behavior typical of many human populations was observed in the three studied municipalities, when compared to other Honduran populations.
Conclusions: The studied communities present high consanguinity due to isolation, ethnic segregation and/or endogamous customs.
Keywords: Genetics; Consanguinity; South American Indians; Names
Determining the degree of inbreeding (approximate average kinship between people in conjugal union) in human populations is important for public health because it is correlated with a high risk of genetic diseases of recessive inheritance.1,2 Two main sources of inbreeding can be defined. The first is observed in small populations subject to strong genetic drift and therefore concurrent genetic homogenization, in which there are few options for mating, i.e. genetic isolation.3 The second is due to cultural features of certain ethnic groups consisting of preference for conjugal unions between members of the same family (endogamous customs), generating genetically distinct groups within communities (stratification).4 In both cases the number of genetic loci in homozygosity is increased. Isolated communities with little immigration and strong genetic drift can be identified through genetic studies using the statistic FST, while stratification within communities can be assessed through the statistic FIS. The total inbreeding due to the two factors is measured through the statistic FIT. Together, these measures are called fixation indices or (alternatively) inbreeding coefficients, depending on the analytical context.5,6
Surnames are inherited like genetic markers on the Y chromosome.7 In a seminal article, Crow and Mange used isonymy (I), i.e. the random probability of marriage between people with the same surname, to assess the likelihood of inbreeding by isolation, noting that I is about 4 times FST. Since then there have been many isonymy studies worldwide, with fine-tuning over time.8,9 Moreover, in countries in Latin America where both names are used, the first inherited from the father and the second from the mother, the calculation of FIS and FIT becomes feasible.10 Since the general trend in various human populations is the avoidance of consanguineous marriages, which leads to decreased inbreeding, isolated FST calculation may result in overestimation of the risk of disorders of recessive inheritance. The possibility to further calculate FIS and FIT is an advantage allowing a more reliable determination of risk.
Studies of the structure of the population of Honduras are recent and mainly relate to DNA loci used in forensic genetics, and the local and national distribution of surnames.10-16 In particular, national isonymy analysis revealed a historical pattern characterized by short-range immigrations and genetic drift, with drift predominating over immigration.10 However, a weakness of the national study is that, due to methodological limitations, the municipality was the minimum population unit considered, which calls for local complementary studies to analyze smaller structural units (villages and hamlets).10
The aim of this study was to evaluate the population structure and determine inbreeding through the consanguinity coefficients FST, FIS, and FIT, applied to the distribution of surnames in 57 communities in three rural municipalities in Honduras, where the population is predominantly mestizo, but with a large component of the Lenca ethnicity. The goal is to confirm the hypothesis that the isolation that determines a high genetic drift in municipalities persists when analyzing smaller population units, and furthermore to explore the existence of endogamous cultural habits in the populations studied. The Lenca are an indigenous population of Mesoamerican origin living in the highlands of three departments of Honduras, Central America: La Paz, Intibucá, and Lempira.17 New ways to graphically display and interpret genetic isolation and inbreeding customs are presented as well.
The study type is observational, descriptive, and cross-sectional with non-probabilistic intentional sampling. The lists of names for analysis were obtained from the Supreme Electoral Tribunal. Honduras has three administrative levels; the country as a whole, divided into departments, divided into municipalities. However, from the population point of view, municipalities are not the lowest structural level; they can be divided into smaller geographical entities like neighborhoods, in the case of urban areas, or villages and hamlets, in rural areas of Honduras. This lower subdivision is included in voter lists and is used in this paper to obtain reliable values of inbreeding coefficients. Usually, a municipality has a major population center that bears the same name as the municipality, with many towns with fewer inhabitants (villages and hamlets).
The municipalities considered for analysis (Figure 1) were: San Manuel Colohete in the department of Lempira, with 20 populated areas; Erandique, in the department of Lempira, with 18 areas; and Yamaranguila, in the department of Intibucá, with 19 areas. A total of 408 different surnames found in the lists of the first and second surnames of 20,712 voters were studied.
Figure 1 Map of Honduras divided by political department. The municipalities studied are: 1. San Manuel Colohete; 2. Erandique; 3. Yamaranguila
Inbreeding coefficient FST
The degree of isolation of a village, a city, or any other populated place is primarily a function of two parameters: 1) the rate of immigration, and 2) the number of inhabitants (in the case of geographical isolation) or effective population size (in the case of reproductive isolation). The smaller the size of a population, the greater the probability that a marriage is inbred. Conversely, the higher the rate of immigration, the greater the exogamy and the lower the probability of intermarriage. However, the proportion of homozygous genetic loci also depends on the time during which a population has been in isolation. A small population size accompanied by a low rate of immigration has the effect of eliminating alleles and fixing others, drastically changing gene frequencies with each generation (genetic drift), reducing variability and increasing homozygosity and thus the risk of recessive conditions.
Random isonymy (RI) measures the historic genetic drift and is simply defined as the random probability of marriage between persons with the same name. The proportion of each surname was calculated for each village. Then RI was computed as the sum of the squares of these proportions. Finally, the FST coefficient for a place is about ¼ RI.10,14-16 The total list of the first plus the second surnames was used for FST calculations. The parameter values are between 0 (for a population in which each individual is unrelated to the others and has a different name from every other person) and 1 (for fixation, that is, one single name in the population).
Inbreeding coefficient FIS
The FST coefficient cannot measure the total inbreeding by itself because of the possibility of structuring the populated area into small, inbred units. While FST estimates the total inbreeding in the event that all marriages are random, real populations tend to show nonrandom mating habits. These customs vary from the full avoidance of consanguineous pairings, to exclusive pairing within families, tribes, or ethnic groups due to cultural, religious, economic, or social factors. An important feature of FIS calculated based on surnames is its ability to differentiate from one another. A negative value indicates avoidance of inbreeding, and positive indicates a population structured into endogamous groups. A value of 0 indicates random pairings (panmixia), and the parameter range is between -1 and 1.10,15,18,19
The value of FIS for a population is equal to ¼ of the nonrandom component of isonymy (IN), calculated as (IT-IR)/(1-IR) where IT is the total isonymy, i.e., the proportion of voters with both surnames the same. To calculate this parameter, voters with only one surname were excluded.
Inbreeding coefficient FIT
This ratio measures the total inbreeding, and takes into account the random component (isolation) as well as the non-random component (mating customs) of inbreeding. For each village, FIT was calculated as FIS + FST (1-FIS).10,15,18,19
Principal component analysis
To visualize how communities cluster and the direction of diffusion of surnames, a principal component analysis (PCA) was conducted using frequencies of surnames with Multibase 2014. The PCA software sorts the elements into certain axes by eigenvectors. Each of these vectors explains a percentage of the variance. The first three components were taken for analysis.
For comparison purposes all analyses were performed in the populations studied and others previously published.15
Diagrams of surname distribution frequency
The frequencies of surnames were used to graphically show the history of the population of each municipality. Briefly, the diagrams constructed based on surname frequencies assume that: 1) the log-log distributions of surnames follow a power law or Pareto, with only a few common surnames and a large number of low-frequency surnames.20 2) the most frequent names correspond to the founders of the population, while the less common are mostly newcomers. A line connecting the points on a graph of surname frequency versus the fraction of the population would represent, from left to right, the history of the peopling of the area.
The proportion of the population with names of different frequencies must remain constant over time in the case where migration has also been constant and with a magnitude in precise balance with genetic drift. In this case, the line would be approximately flat and horizontal. Therefore, any fluctuation in the "flatness" of the line would correspond to fluctuations in the peopling process. A high beginning, along with a negative slope and a low end, show a predominance of genetic drift over migration, and vice versa. In addition, peaks represent waves of immigration.21
Inbreeding coefficients of the 57 populated areas included in this study are shown in Table I. The FST values (which measures the effect of historical isolation and genetic drift) ranged from 0.0083 to 0.0467. The most isolated communities were Tierra Colorada, El Conal, and El Carrizal, all located in Erandique, with FST values above 0.05. The lowest values were found in Erandique, Azacualpa Grande, and Joscamón, also belonging to Erandique, showing greater variation in the degree of isolation between places within this municipality, compared to the rest.
|Table I Coefficients of intermarriage in 57 Honduran communities|
|San Manuel Colohete1||837||-0.0085||0.0210||0.0126|
|San Isidro or El horno1||292||-0.0232||0.0269||0.0043|
|San Antonio del aguacatillo1||85||-0.0007||0.0270||0.0263|
|San José del naranjo1||136||-0.0078||0.0304||0.0229|
|San Antonio montaña2||503||0.0027||0.0175||0.0201|
|Valle de la cruz2||323||-0.0082||0.0367||0.0288|
|Concepción or barrio nuevo2||391||-0.0067||0.0249||0.0184|
|El rodeo 22||157||0.0026||0.0307||0.0332|
|El tablon no. 23||220||-0.0086||0.0208||0.0124|
|El membrillo no. 13||391||-0.0076||0.0242||0.0168|
|N = number of voters; 1San Manuel Colohete; 2Erandique;3Yamaranguila|
Forty-one areas presented negative FIS values and two practically zero (< 0.002). This result indicates that for the most part there is no additional structuring in the villages and hamlets, i.e., population subdivision into units within which pairings are more frequent than in the rest of the populated area. Rather, people prefer marriages with unrelated individuals (avoidance of inbreeding), indicating that the level of geographic subdivision considered for analysis is adequate for these sites. However, the other places showed positive values equal to or above 0.002. This structure may be due to endogamous customs (marriages between relatives), or alternatively, because the populated areas are made up of ethnic groups that mix very little with each other. The areas with the highest FIS were Tierra Colorada, Yolomón, and Gualguirre, while those with the highest FIT values (which shows the total inbreeding) were found in Tierra Colorada, El Carrizal, and El Conal.
In order to interpret the causes of the high FIS values, these were analyzed together with FST. Figure 2 shows plots of FIS versus FST in the three municipalities studied and five previous studies.15 Interestingly, Brus Laguna, Juan Francisco Bulnes, Iriona, and Orica show FIS that tends to behave as a linear function of FST. In these four municipalities, FIS has a strong tendency to decrease with isolation. The graphs show what appears to coincide with a natural tendency of human populations to avoid inbred pairings; for example, the more genetically homogeneous a population due to historical isolation, the more actively individuals avoid inbred pairings.
Figure 2 FST (X axis) versus FIS (Y axis) in eight Honduran municipalities. Each point represents a community. Municipalities in the top row show exogamous behavior characterized by a high negative correlation between FST and FIS. The municipalities of the lower row contain many communities with endogamous customs or, alternatively, ethnic segregation, denoted by poor correlation, steepening, and/or shift to the right of the trendline, and high dispersion
The picture is different in Trinidad, San Manuel Colohete, Erandique, and Yamaranguila. Here, the graphs are characterized by a low correlation between FST and FIS, a high dispersion of points, and a shift in the trend line to the right, indicating a high variation in marriage customs due to the variable European/Amerindian composition between villages. In particular, the shift to the right and many positive FIS values, along with high FST values, indicate the existence of areas in the four municipalities with strong endogamous customs.
For Figure 3, an oblique line was plotted from the origin with a slope of -1. The communities located along those lines would, in theory, have perfect exogamous behavior (which could be defined as the magnitude of the trend of human populations to avoid pairings between relatives), so as to offset the effects of genetic isolation, bringing the total inbreeding values to zero. The villages located on and below this line then should present exogamous behavior that is likely to largely counteract the effects of inbreeding by isolation, with the number of homozygous genetic loci dropping as a result, thus decreasing the prevalence of recessive diseases. Such is the case of most communities in municipalities of African descent (Juan Francisco Bulnes, Brus Laguna, and Iriona), and Orica. On the other hand, communities that are between this oblique line and the X axis probably have a high genetic risk despite having negative FIS values, since its magnitude is not enough to counteract the effects of inbreeding by isolation. Finally, communities that are above the X axis exhibit plainly endogamous behavior. Most communities in this study are located in the last two zones, showing increased genetic risk.
Figure 3 FST (X axis) versus FIS (Y axis) in eight Honduran municipalities. Each point represents a community. Municipalities are colored according to their ethnic affiliation. The diagonal line represents the ideal exogamous trend, with FST and FIS correlation equal to 1. Each community is in one of three areas: the exogamous where the negative magnitude of FIS compensates for intermarriage due to high isolation, near or below the diagonal; the exogamous who do not compensate for isolation, between the diagonal and the X axis; and the communities with high intermarriage, above the X axis
Whether the intermarriage customs are owed to the European component, the indigenous, or both, is difficult to determine, as the customs, the segregation, and the percentages of ethnic composition could co-vary in a complex, nonlinear manner in these territories (there is however evidence of strong endogamous customs in the Sephardic population of European descent in Trinidad).15 The evaluation of differential marriage customs in the three municipalities studied requires a subsequent detailed demographic analysis.
Figure 4 graphically depicts the populated areas using PCA. The first three dimensions were graphed, which explain 44% of the variance. Clearly PC1, which represents almost 28% of the variance, separates the three municipalities of Lenca descent from the rest (as mentioned, three of African descent and one of Jicaque indigenous descent), indicating low migration between the two groups. The communities within each municipality tend to cluster together; however, the dispersion varies between the municipalities. For example, Erandique communities are more dispersed than those of San Manuel Colohete and Yamaranguila, demonstrating a higher level of isolation for the towns in Erandique.
Figure 4 Principal Component Analysis (PCA). The first three components are shown. Each point is a community. The components (represented by each axis) range from low to high variability of surnames
Taken as a whole, the communities of San Manuel Colohete do not show a clear separation with Erandique, while Yamaranguila is separate from the two (PC2). Since each component is distributed along the axis according to the variability of surnames, the graph is consistent with the distribution of surnames from the Honduran coast (communities of African descent) inland (indigenous communities), most evident in PC1 and PC2, reflecting national-level findings.10 It is striking that San Manuel Colohete overlaps with Trinidad, a community with strong Sephardic influence, with a diffusion of surnames observable along PC1 from Trinidad to San Manuel Colohete. Suspicion of a close relationship between the two communities is increased with the recent discovery of an important Sephardic cultural component in San Manuel Colohete.22
Figure 5 shows diagrams of surname frequency distributions for the three municipalities studied plus Iriona (added for comparison). Each diagram shows the historical settlement of a municipality as a whole. In all three, the common surnames are carried by a very high proportion of the population and the uncommon ones by very few people. This results in curves typical of isolated populations with an initial settlement followed by high genetic drift and little historic (or recent) immigration. In contrast, the municipality of Iriona (largely inhabited by the Garifuna ethnicity of African descent) shows a strong initial drift, but also relatively high recent immigration, with many smaller waves of immigration represented by historic peaks.
Figure 5 Diagrams of distribution frequency of surnames. The X-axis represents the proportions of surnames, and the Y axis the percentage of the population
Isonymy studies are helpful in evaluating the structure of human populations, and now have gained new momentum with the availability of large amounts of data contained in the electoral or civil registers of different countries. The study of isonymy has proved particularly effective in determining the predominance of immigration over genetic drift or vice versa, and therefore for the assessment of genetic isolation and the risk of recessive disorders,23 with the advantage in Latin America of also being able to calculate the additional risk arising from mating customs. In this study the fragmentation of territory to the lowest possible level by estimating FIS reveals a partly segregated territory, populated by some highly endogamous groups.
Preferential mating customs between relatives and genetic isolation are not uncommon, and it is estimated that about 10% of the world population is the result of inbred marriages.24 In ancient societies with a history of high proportions of intermarriage, enough time will have passed for the mechanism of natural selection to purge many harmful alleles that cause recessive genetic disorders.25 However, in populations that have experienced a recent reduction in number or have recently migrated to establish new settlements (such as those studied here), the founder effect and genetic drift can randomly raise the frequencies of some harmful allele.26 In these conditions the risk of recessive genetic diseases can increase, especially in children of intermarriage.
In Honduras, during the time of Spanish conquest and domination, European immigrants settled in the fertile valleys while partaking in a process of mestizaje or racial interbreeding. Several indigenous groups, fearing war and eager to preserve their customs, including the Lenca, were displaced to higher ground where they still retain many of their customs.27 Among the indigenous groups in Honduras, the Lenca is the largest, with around 217,000 people living in the mountainous areas of southwestern Honduras. Most still live isolated in small towns in conditions of extreme rural poverty.28
The Lenca, as well as many other ethnic populations in the Americas, are at high social risk due to several factors that affect their health, including social segregation, geographic isolation, poverty, scarcity, and poor-quality health services.29 In rural areas of Honduras, a child affected with a genetic disorder may not only represent a huge financial burden for the family, but moreover their chances of survival are minimal. Therefore, any effort to prevent such diseases can have a positive impact on the population. In this paper we demonstrate beyond a doubt that the communities studied are in isolation, but more importantly, many of them have strong intermarriage customs. This knowledge may enable public health providers and other institutions, such as NGOs, to intervene by providing appropriate genetic counseling to local people. However, isonymy studies complement but do not replace genetic epidemiological studies, and additional work is needed to determine the prevalence of different genetic conditions in the Lenca populations of Honduras.
Apart from the existence of highly endogamous communities in the territories studied, a general trend in most populations shows the avoidance of intermarriage. This paper shows that the magnitude of this "impulse" to strive to make the nest outside the family circle is greater, the greater the isolation, following a linear trend. It is interesting that this behavior is finely regulated in such a way to offset the effects of the random component of inbreeding. A similar result can be found in the work of Baldi et al. in seven communities of the Rama ethnic group of Nicaragua, where isolation was observed accompanied by the avoidance of inbreeding, with FST values highly negatively correlated with FIS.30 The genetic and psychosocial factors driving this natural tendency, which may be modified by structuring because of behaviors associated with cultural systems leading to preferential mating, deserve to be explored in greater depth. Finally, the results of the high negative correlation of FST and FIS indicate that it is likely that studies including FST as the only statistic to explore territories in search of populations with genetic risk, are after all not sufficient, since many (if not most) genetic isolations instinctively avoid recessive diseases through these behaviors.
The author thanks Attorney Carlos Humberto Arita Mejía, of the Supreme Electoral Tribunal of Honduras, for granting the data.
Conflict of Interest Statement: The author declared that there is no personal or institutional conflict of interest of a professional, financial, or commercial nature, during the planning, execution, writing of this article..