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Modelling the prehistoric geographical distribution of the genus Meleagris
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Modelling the prehistoric geographical distribution of the genus Meleagris Eduardo Corona-Ma,∗, José Alberto Cruz Silvab a
Instituto Nacional de Antropología e Historia, Centro INAH Morelos, Matamoros 14, Col. Acapantzingo, Cuernavaca, 62440, Mexico Benemérita Universidad Autónoma de Puebla. Laboratorio de Paleontología, Facultad de Ciencias Biológicas, Blvd. Valsequillo y Av. San Claudio, 112 A, Ciudad Universitaria, Col. Jardines de San Manuel, Puebla, 72570, Mexico
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ARTICLE INFO
ABSTRACT
Keywords: Wild Turkey Meleagris Biogeography Mexico Late Pleistocene Domestication
Studies of the domestication of animals in the Americas suggest strong relationships between humans and a large number of animal species, with the application of many management strategies. Two species of the endemic pheasant genus Meleagris live in America: the wild turkey (Meleagris gallopavo), culturally the most well-known species, with a natural distribution from North America to central Mexico; and the ocellated turkey (Meleagris ocellata), endemic to the Yucatan Peninsula. However, the cultural exchange of both species, which began with the first sedentary human societies, has obscured the natural distributions of both species in central and southern Mexico. We have modelled the geographical distribution of both species based on the amplitude of the ecological niche, a concept that facilitates our understanding of biological adaptations. The models use temperature, precipitation and current distribution data to project back to the late Pleistocene. Three main inferences can be derived from our models. First, during the late Pleistocene both species of Meleagris experienced a reduction and drastic change in their geographical distribution. Second, the speciation events of the genus Meleagris occurred before the late Pleistocene. Third, the subspecies Meleagris gallopavo gallopavo displays the highest niche amplitude, spanning all other M. gallopavo subspecies, suggesting that it could be a product of cultural management.
1. Introduction Mexico is a country with high biological diversity and a large number of endemic species: the 1097 bird species in Mexico represent about 10% of bird species globally (Howell and Webb, 1995). Undoubtedly, this abundance fostered an intense relationship between the ancient cultures of Mexico and birds. For Mesoamerica, particularly in central Mexico, 360 bird species are known, of which 223 have more than one recorded use. In other words, 20% of the overall Mexican bird species count, and more than 60% of the bird species from central Mexico alone, were used culturally in the transition from late prehispanic to early Colonial times, in 16th century (Corona-M., 2002; 2013a). In recent years, the issue of species domestication by prehispanic cultures in America has resurfaced, introducing debates about the chronology, original distribution of wild species, and changes arising from human influence. Examples of plants under discussion include corn, beans and chilli (Gaut, 2014; Kraft et al., 2014; Ramos-Madrigal et al., 2016). An example from animals includes an intensification of research into turkey species (Meleagris spp.) (Mock et al., 2002; Speller
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et al., 2010; Corona-M., 2013b; Thornton et al., 2016; Manin et al., 2018; Padilla-Jacobo et al., 2018). Recent archaeozoological findings have shown an early trade in these species in preclassic Mesoamerica (Thornton et al., 2012; Martínez-Lira and Corona-M., 2016; Manin et al., 2018), producing several migratory paths influenced by human groups. This early trade marked the beginning of the dispersal of the wild turkey (Meleagris gallopavo) across practically the whole world. Currently, the leading agro-industrial producers of turkey are the United States, Brazil, Germany and France, representing 66% of the global turkey meat output, while in Mexico the turkey represents barely 2% of national meat production (Johnson, 2018). The wild turkey is one of the most used birds in the global diet, yet we know little detail about its diachronic and spatial dispersal. Current analyses of ancient and modern DNA, stable isotopes and radiocarbon dating provide new data that can be used to help explain the various stages of animal domestication. These methodologies also provide us with an insight into the diversity of strategies that together form the continuous process of domestication, ranging from the management of wild species, through methods of extracting offspring,
Corresponding author. E-mail address: [email protected] (E. Corona-M).
https://doi.org/10.1016/j.quaint.2020.03.053 Received 1 July 2019; Received in revised form 24 March 2020; Accepted 25 March 2020 1040-6182/ © 2020 Elsevier Ltd and INQUA. All rights reserved.
Please cite this article as: Eduardo Corona-M and José Alberto Cruz Silva, Quaternary International, https://doi.org/10.1016/j.quaint.2020.03.053
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Fig. 1. Comparative of current distribution of Meleagris species and subspecies. A) Current distribution of the turkey species Meleagris gallopavo (diagonal lines) and Meleagris ocellata (white area) (data from CONABIO, modified from Navarro and Peterson, 2007). B) Model of potential current distribution of the turkey species M. gallopavo (diagonal lines) and M. ocellata (white area), based on data of this study. C) Current records for M. gallopavo (white triangles) and M. ocellata (white circles), D) Current records for subspecies of M. gallopavo including M. g. gallopavo (circle), M. g. intermedia (triangle), M. g. merriami (cross), M. g. mexicana (square), M. g. silvestris (diamonds) and M. g. osceola (star). Maps 1C and 1D, see material and methods section. D.
captivity and taming, to the production of particular lineages of specific interest to human groups. Differences in these strategies may be associated with the availability of specific animal populations or subpopulations, resulting in the same species displaying different chronologies and domestication events, as has been observed in several ‘traditional’ domestic species, such as horses, dogs and cats (Larson et al., 2014; Vigne, 2015; Zeder, 2017). Animal domestication in Mesoamerica is an understudied subject, and addressing it through a particular case study will serve as a model that could be expanded to other animal groups widely used in prehispanic cultures, such as dogs, deer, rabbits and hares. Seeking to understand wildlife management in past Mesoamerican societies, we have therefore used turkeys as such a case study. The turkey is an endemic American pheasant that includes two species from the genus Meleagris: the wild turkey (Meleagris gallopavo), which is distributed naturally from North America to central Mexico; and the ocellated turkey (Meleagris ocellata), restricted to the Yucatan Peninsula and scarcely known beyond its current location in natural environments and even within its original geographical distribution (Corona-M., 2013b; Manin et al., 2018) (Fig. 1). The wild turkey has received considerable attention in archaeological studies because of its wide geographical distribution in association with diverse American cultures. The oldest specimens of wild turkey in Mexico are found in late Pleistocene contexts on the Mexican Plateau, while the ocellated turkey does not have any Pleistocene records (Corona-M., 2009). Little is known about its speciation process. In the last ten years, significant advances have been made in the development of algorithms that allow modelling of the ecological niche of a species based on a variety of conditions, such as temperature, climate, diversity of foods and range of habitats that a species could inhabit. Recent applications include identifying changes in biogeographical ranges in response to climate change, enhancing our
understanding of biological adaptations (Sexton et al., 2017). Ecological modelling enables quantification of the ecological niche of particular species, and evaluation of the effect of climatic changes and deforestation on biodiversity. However, its most frequent application is modelling the geographical distribution of a particular taxon (Guisan and Thuiller, 2005). This study provides models for the geographical distribution of both species of Meleagris and the subspecies of M. gallopavo in Mexico, based on the amplitude of the ecological niche using temperature, precipitation and current distribution data. We followed a two-step process: first, we obtained current distribution data for the study taxa; second, we factored in the influence of climatic variables on the geographical distribution. Based on this information, models for probable late Pleistocene distributions were then proposed. 2. Material and methods Presence records were obtained from the databases of the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (www. conabio.gob.mx) (Fig. 1A), Global Biodiversity Information Facility (www.gbif.org) and Integrated Digitized Biocollections (www.idigbio. org) for Meleagris ocellata, and for Meleagris gallopavo and its subspecies (M. g. gallopavo, M. g. intermedia, M. g. merriami, M. g. mexicana, M. g. osceola and M. g. silvestris). Records were reviewed and included only if they were supported by specimens in a scientific collection; sightings only were excluded. These were analysed with QGIS (QDC Team, 2018) and validated using the natural distribution of turkeys indicated by the databases and published sources (Fig. 1B) (Steadman, 1980; Speller et al., 2010). The two-step process of the analysis excluded records of extinct or palaeontological species because they did not have associated reliable climatic records or their phylogenetic relationships were uncertain. However, any future 2
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analysis could factor in those effects. For the subspecies South Mexican turkey (M. g. gallopavo), because of the uncertainty of its natural distribution, the records used had to match two conditions: located in central Mexico, and with specimens in scientific collections identified or referred to as wild, i.e. specimens without evidence of human management. This approach led to the inclusion of fewer records but increased the reliability of the results. The presence records and climatic variables were analysed using Maxent 3.4.0 (Phillips et al., 2006, 2017). The basis of this program is the concept of maximum entropy, in order to make predictions from incomplete information. Maxent estimates the most uniform distribution throughout the study area with the restriction that the expected value for each environmental variable agrees with its empirical average, i.e. the average values for the occurrence data set (Phillips et al., 2006, 2017). Five potential distribution models were made with bootstrapping for each of the taxa, and the one with the best performance was selected. The parameters used were random test percentage = 30% and regularization multiplier = 1, discarding the clamping option. The model fit estimator area under the curve (AUC) was chosen, using the highest value, because it is not threshold dependent, unlike other evaluation metrics such as sensitivity, specificity and true skill statistics (TSS), and is therefore considered a more reliable metric for comparing results from different ecological niche models (García–Roselló et al., 2019). The resulting models were analysed further with QGIS, to obtain binary values for presence (1) and absence (0) for each of the species and subspecies, using the ten percentile training presence as a threshold. The ecological niche models revealed the contribution of climatic variables, such as the values of average annual temperature and annual precipitation, to the potential distribution of each taxon. The Last Glacial Maximum (LGM) models (ca. 21,000 years BP) were based on projections of the presence records and the climatic variables available in Worldclim version 1.4 (www.worldclim.com), and also on the MIROC-ESM global climate model (www.ecoclimate.org/ downloads). Comparisons between ancient and current potential distributions provide us with an understanding of the geographical changes from the LGM onwards (Varela et al., 2015).
Table 1 The relative contribution (%) of the bioclimatic variables used in the ecological niche models for Meleagris gallopavo and Meleagris ocellata. Bold values indicate the variables with the highest importance for the modelled potential distributions. Climatic variable
M. gallopavo
M. ocellata
Bio1: Annual mean temperature Bio2: Mean diurnal range Bio3: Isothermality Bio4: Temperature seasonality Bio5: Max temperature of the warmest month Bio6: Min temperature of the coldest month Bio7: Temperature annual range Bio8: Mean temperature of wettest quarter Bio9: Mean temperature of the driest quarter Bio10: Mean temperature of warmest quarter Bio11: Mean temperature of coldest quarter Bio12: Annual precipitation Bio13: Precipitation of wettest month Bio14: Precipitation of driest month Bio15: Precipitation seasonality Bio16: Precipitation of wettest quarter Bio17: Precipitation of driest quarter Bio18: Precipitation of warmest quarter Bio19: Precipitation of coldest quarter
0.2 1.8 0.1 7.0 13.2 44.5 2.8 3.0 6.2 1.2 1.4 0.3 9.9 0.3 0.9 0.0 0.1 1.6 5.5
1.4 0.3 24.2 19.2 0.1 26.1 9.4 1.6 0.7 0.2 9.1 0.0 1.5 4.2 0.1 0.2 0.8 0.3 0.6
Bio6, Bio7 and Bio11 variables suggested a more stable environment, very similar to the restricted habitats of humid forests and brushy woodlands that occur in the Yucatan Peninsula (Howell and Webb, 1995). However, despite these differences in the climatic conditions, both species shared the variable related to the minimum temperature of the coldest month (Bio6). Remarkably, of the climatic variables that were most influential in constructing the models for both species, only precipitation was of relative importance geographically for the wild turkey. To observe any differences between the climatic niches of each species, the values for annual average temperature and annual precipitation were extracted from the potential distribution. For average annual temperature, the climatic niche of the wild turkey was broader, ranging from 1.5 °C to 25 °C, while for the ocellated turkey it was narrower, ranging from 22.5 °C to 26.6 °C. (Fig. 2). It is important to note that the overlap in average annual temperature values for the two species was very small. The breadth of the climatic niche was wider for the wild turkey, as indicated by the annual average temperature. However, the overlap of annual precipitation values was wider between the two species (Fig. 2). For annual precipitation, the wild turkey had a higher tolerance to drier conditions (less than 700 mm) than the ocellated turkey, which had a higher tolerance of more humid environments.
3. Results and discussion We obtained 621 unique records for M. gallopavo and 677 records for M. ocellata (Fig. 1C). For the subspecies of M. gallopavo, the records numbered M. g. gallopavo (10), M. g. intermedia (97), M. g. merriami (61), M. g. mexicana (35), M. g. osceola (37) and M. g. silvestris (273) (Fig. 1D). 3.1. Distribution and climatic niche of Meleagris species The models for the current potential distribution of M. gallopavo and M. ocellata did not overlap (Fig. 1A and B). The areas were smaller than those shown in Fig. 1A, which is the distribution as determined by the Commission for the Use and Management of Biodiversity (CONABIO in Spanish) (Navarro-Siguenza and Peterson, 2007). These differences may have arisen because our database did not include sighting-only records, which could lead to geographical over-representation. However, if this distribution provides a better fit to the environmental conditions that determine the niche, then this reduction in habitat may illustrate the current Anthropocene conditions better, such that we are observing habitat fragmentation and smaller areas than previously published. The climatic variables making the most significant contribution to the current geographical distribution models differed between the two species (Table 1). For the wild turkey, a combination of Bio5, Bio 6 and Bio13 variables suggested tolerance of a broad range of temperature and precipitation, which explained its wide distributional range in North America. For the ocellated turkey, the combination of Bio3, Bio4,
3.2. Distribution and climatic niche of Meleagris gallopavo subspecies Ecological niche models for the distribution of each subspecies of the wild turkey showed a clear separation for most of them, suggesting that climatic conditions had the most influence on their geographical distribution (Fig. 3A). However, there are two exceptions worthy of discussion. First, the Gould turkey (M. g. mexicana) has a potential distribution that falls within that of the Merriam turkey (M. g. merriami) (Fig. 3A), suggesting a close relationship between them. A possible explanation for this is provided by Manin et al. (2018), who show that these two subspecies are very close phylogenetically and share the H2 haplotype, which in biogeographical terms also suggests a close interaction between these subspecies. This raises the question of whether the geographical distribution encompassing both subspecies is a product of trade and management by ancient human cultures in this area. The management of the Gould turkey in two cultural areas, Mesoamerica and Oasisamerica, is of 3
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Table 2 The relative contribution (%) of the bioclimatic variables used in the ecological niche models for the Meleagris gallopavo subspecies. Bold values indicate the variables with the highest importance for the modelled potential distributions. See Table 1 for the definitions of the bioclimatic variables. Climatic variable
M. g. gallopavo
M. g. intermedia
M. g. merriami
M. g. mexicana
M. g. osceola
M. g. silvestris
Bio1 Bio2 Bio3 Bio4 Bio5 Bio6 Bio7 Bio8 Bio9 Bio10 Bio11 Bio12 Bio13 Bio14 Bio15 Bio16 Bio17 Bio18 Bio19
22.9 0.1 1.4 0.3 0.0 43.4 1.4 10.2 0.1 0.0 13.7 0.2 0.0 0.0 0.0 0.0 0.0 0.7 5.6
0.4 1.0 0.0 5.2 0.4 15.2 1.4 0.4 10.3 36.7 10.7 0.2 0.0 5.6 8.4 0.0 0.9 2.4 0.8
5.5 12.6 48.4 6.0 3.1 0.0 0.3 2.7 0.8 4.1 4.6 0.1 2.9 0.8 3.7 0.2 1.6 1.3 1.3
8.1 6.0 35.0 2.3 0.1 6.9 0.4 0.2 0.9 0.2 3.6 0.1 5.3 3.8 11.8 1.2 1.7 6.9 5.7
0.4 0.0 1.7 12.6 0.0 0.3 0.3 11.8 0.2 0.5 0.0 0.0 0.8 5.0 7.2 0.0 0.0 59.1 0.1
1.1 0.2 0.2 4.5 2.4 4.8 0.6 1.6 1.2 17.3 4.6 4.0 0.0 5.6 11.6 0.6 35.6 3.8 0.1
and the Merriami turkey (M. g. merriami). For the rest of the M. gallopavo subspecies, at least one precipitation variable was indicated (Table 2). For the subspecies in eastern North America, the Florida turkey (M. g. osceola) and Eastern turkey (M. g. silvestris), precipitation of the warmest quarter (Bio18) and precipitation of the driest quarter (Bio17), respectively, contributed most to their modelled distributions (Table 2), suggesting a more humid environment. All of these results were consistent with a possible differentiation of climatic niche between the subspecies of M. gallopavo. When extracting the average annual temperature values for each of the subspecies of wild turkey, the Mexican turkey (M. g. gallopavo) presented a broad overlap and encompassed practically all the climatic niches of the rest of the subspecies. This suggests that a high tolerance to different climatic conditions is the product of interactions with humans (Fig. 4). There is a clear differentiation in the amplitude of average annual temperature for the Rio Grande turkey (M. g. intermedia) and Florida turkey (M. g. osceola), because they are located in areas with higher temperatures compared with the rest of the subspecies. For the Merriami (M. g. merriami), Gould (M. g. mexicana) and Eastern (M. g. silvestris) turkeys, extensive overlaps between the average annual temperature values exist (Fig. 4). These three subspecies are located in central North America and reach the east and west coasts of Mexico. The human cultures in those areas interacted significantly with these
Fig. 2. Climatic values of mean annual temperature (° C) and annual precipitation (mm) in geographical ranges of M. gallopavo (dashed line) and M. ocellata (continuous line).
particular interest, but addressing this lies outside the scope of this paper. Second, the other subspecies of interest within a Mesoamerican context is the Rio Grande turkey (M. g. intermedia), with a current distribution extending towards eastern Mexico and the United States but not reaching central Mexico. This model suggests that the expansion of the Rio Grande turkey is the result of trade and cultural traffic. The most unusual and broadest potential distribution is that of the subspecies South Mexican turkey (M. g. gallopavo), which encompasses the distribution of all other subspecies and beyond towards the south (Fig. 3B). Archaeological samples of this subspecies share haplotypes (Hap 1 and Hap 2) and are found in practically all regions of Mexico apart from the north (Manin et al., 2018). This result raises the question of whether the geographical distribution of this subspecies is a product of its management, expanding rapidly because of its association with human cultures. The data suggest that this is a highly probable event, but further phylogeographic research is needed to explore this fully. Regarding the percentage contribution of climatic variables to the ecological niche models for each subspecies (Table 2), temperature variables contributed the most for the Mexican turkey (M. g. gallopavo)
Fig. 3. Distribution of Meleagris gallopavo subspecies. A) M. g. intermedia (front diagonal lines \\), M. g. merriami (vertical lines), M. g. mexicana (white area), M. g. osceola (back diagonal lines///) and M. g. silvestris (horizontal lines). B) M. g. gallopavo (white area). 4
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Fig. 4. Climatic values of mean annual temperature (° C) and annual precipitation (mm) in geographical ranges of. gallopavo subspecies including M. g. gallopavo (continuous black line), M. g. intermedia (dotted grey line), M. g. merriami (continuous grey line), M. g. mexicana (dashed black line), M. g. osceola (dashed grey line) and M. g. silvestris (dotted black line).
three subspecies, and the climatic conditions possibly favoured their management and trade. When examining the data for average annual precipitation, the Mexican turkey shows similar results as for temperature, with this subspecies spanning the curves of practically all other subspecies and indicating a tolerance of more humid environments, including those with more than 800 mm of rainfall (Fig. 4). However, in spite of the overlap in precipitation curves, some differentiation is evident (Fig. 4). The Merriami and Gould turkeys tolerate the driest habitats, which is congruent with their location in the Highlands of North America and Mexico. The Florida and Eastern turkeys prefer the more humid environments in eastern North America, while the Rio Grande turkey tolerates intermediate values of average rainfall and its distributional range falls between those of the Florida and Eastern turkeys (Figs. 3 and 4).
for North America and Mexico (Steadman, 1980; Corona-M., 2009). A disjunct population is modelled in the southeastern United States, where a continuum might have been expected, as is also the case today. Two hypotheses could explain this. First, a population covering a greater distributional range before the LGM was split towards the end of this period, perhaps as a result of changes in vegetation, as the models indicate that some populations of wild turkey are susceptible to climatic variables. Second, in the early Holocene, the separated wild turkey populations were able to rejoin across the original distributional area, but with distinctive haplotypes, as suggested by the populations of Florida and Eastern turkeys. This raises the possibility that both subspecies are the product of changes in the early Holocene, which is certainly an issue for further research. For the ocellated turkey (M. ocellata), the model suggests its presence in the east and south of the Yucatan Peninsula. If we consider the vegetation extant before intensive human use, this is an area of humid forests, while dry forest is located to the northwest of the peninsula (Durán García and García Contreras, 2010). A hypothesis therefore arises of an original association of the ocellated turkey with humid vegetation. In that case, the areas indicated by the model also suggest a reduction in distribution in eastern Yucatan Peninsula, with a shift towards the south and a division into two areas that comprise the east of the Yucatan Peninsula and the flood zone of the state of Tabasco, where currently the species is not found naturally. The possible presence of a separate population could be explained by a reduction in the range of a
3.3. A late Pleistocene models of Meleagris species and subspecies The ecological niche distributional models were projected to the late Pleistocene, in particular to the LGM (ca. 21,000 years BP). For the wild turkey (M. gallopavo) the model shows a narrower distributional range than models for the present-day. The distribution indicates the presence of wild turkey in the Highlands of North America and Mexico, but it does not reach central Mexico (Fig. 5). This matches the distribution of most of the late Pleistocene records for the genus Meleagris 5
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Fig. 5. Potential distribution inferred for the late Pleistocene (~21,000 years BP) in the Last Glacial Maximum. Pleistocene distributions of M. gallopavo (front diagonal lines \\) and M. ocellata (vertical lines) compared to the current distributions of M. gallopavo (back diagonal lines///) and M. ocellata (horizontal lines).
large ancient population that originally covered the whole area, and, near the LGM, an extirpation of the population in the Tabasco area. This model is congruent with evidence provided by pollen studies that shows climatic and dynamic vegetational changes from the late Pleistocene to the Holocene (Gill, 2014; Gill et al., 2014). In some areas of the Yucatan Peninsula, changes from medium to low stature forest have been documented by 7500 cal years BP, and later changes from moist to drier conditions (Carrillo-Bastos et al., 2010). Finally, throughout the Holocene, the surviving population of ocellated turkey consolidated its presence and expanded to cover all types of vegetation across the Yucatan Peninsula, i.e. tropical deciduous forest, humid forest and a later humanized habitat known as milpa, where it is found currently (Howell and Webb, 1995). However, in the last few decades, with a reduction in their range because of the growth of the human population, the species is facing a severe extinction risk (Kampichler et al., 2010). The habitat changes of the ocellated turkey therefore need further urgent review. Another question arising is when the original population of the genus Meleagris split into the current two species. Any hypothesis needs to include the ancient and large turkey population, from the early Pleistocene or earlier, that inhabited the north of America and the east of Mexico, including the Yucatan Peninsula, which may have been associated with brushy woodland and temperate woods. Across different episodes of climatic and vegetational change, this population suffered fragmentation and local extinctions, the data from our model updating Steadman's (1980) proposal. The origin of ocellated turkey as a species could therefore be located in the Blancan or Irvingtonian time periods. Comparing the late Pleistocene models for wild turkey subspecies show interesting distributional changes. The most remarkable is the Mexican turkey subspecies (M. g. gallopavo), which shows an extensive distributional range, from southern Mexico through to the Panama Bridge and northern part of South America, while to the west it includes the Caribbean (Fig. 6E). This is an unusual result as no record of any wild turkey exists in these areas from that time. This model may therefore be reinforcing the hypothesis given above that the Mexican turkey population is a product of cultural management. Another compelling case is the Florida turkey (M. g. osceola), for which, after modelling, there does not appear to have been optimal climatic conditions during the Pleistocene. It is possible that this
subspecies split from ancient Eastern (M. g. silvestris) or Rio Grande (M. g. intermedia) turkey populations that expanded to Florida during the early Holocene (Fig. 6A and D). The first option is consistent with the evidence provided by Mock (2002). The distribution of the Rio Grande turkey shows a southern displacement in its present range compared with the ideal climatic conditions for this subspecies in Florida (Fig. 6A). The range of the Merriami turkey (M. g. merriami) has changed, losing areas in which it is currently present, but also expanding in eastern America, particularly in the western United States and in Mexico from the northwest and to central Mexico in the Highlands (Fig. 6B). Finally, the model for the Gould turkey (M. g. mexicana) suggests a broad area of distribution in southern North America and north of Mexico in the Highlands (Fig. 6C). Both the present and Pleistocene populations of the Merriami turkey overlap with the range of Gould turkey, and it is probable that before the LGM they were neighbouring populations. An expansion of the Merriami turkey could have caused the overlap. It is interesting that these two subspecies are associated with management processes in Oasisamerica, while the Gould turkey is also associated with cultures in Mesoamerica, as illustrated by Manin et al. (2018). 4. Final considerations The wild turkey population in the LGM model inhabited the southern part of North America. It is probable that the influence of climatic events near the LGM fragmented the population on an east–west axis, located in the Highlands and limited by the Sierras Madre in Mexico. This phenomenon has been observed in several species of birds (Corona-M., 2009) and is illustrated by the models for subspecies of wild turkey here discussed. The evidence also suggests that the Meleagris speciation events occurred before the LGM. Based on the palaeontological record, the genus can be traced back to the Blancan or Irvingtonian time periods, during which many phenomena that changed the configuration of American biodiversity have been detected, such as the Great American Biotic Exchange (Corona-M., 2009). These issues should therefore be part of further modelling. The models obtained for the two species, for both the present and 6
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Fig. 6. Potential current distribution (back diagonal lines///) and inferred distribution for the late Pleistocene (~21,000 years BP) in the Last Glacial Maximum (front diagonal lines \\) of the subspecies of M. gallopavo. A) M. g. intermedia, B) M. g. merriami, C) M. g. mexicana, D) M. g. silvestris, E) M. g. gallopavo, and F) M. g. osceola shows only the current distribution since the Pleistocene does not have optimal climatic conditions for an ecological niche model.
the LGM, allow us to confirm the hypothesis that the natural distribution of the wild turkey is in the Highlands of Mexico and North America, where a temperate climate predominates, associated with the Nearctic region. Their southern limit appears to be in the Mexican Neovolcanic Axis (Corona-M., 2009), and the distributional range of wild turkey in all models, current and Pleistocene, extends to this southern limit. This suggests that the records of wild turkey in the preclassic of central and southern Mexico are a product of trade and management (Thornton et al., 2012; Corona-M., 2013b; Martínez-Lira and Corona-M., 2016). It is interesting to note the dynamics of expansion and shrinkage in the distribution of the species and subspecies of Meleagris during the Pleistocene–Holocene transition. Our modelling introduces the LGM as a boundary for discussing a number of hypotheses about ancient distributions and splits of turkey populations. In particular, these models show considerable congruence with genetic evidence (Mock et al., 2002; Speller et al., 2010; Speller and Yang, 2015; Manin et al., 2018) and suggest that the distributional ranges are
a product of climatic changes from the late Pleistocene (LGM) onwards. The subspecies most likely to have interacted with early cultures are the Rio Grande (M. g. intermedia), Merriami (M. g. merriami) and Gould (M. g. mexicana) turkeys, as also indicated by the archaeogenetic record (Manin et al., 2018). The Mexican turkey subspecies (M. g. gallopavo) appears to be a eurioic population, with high environmental plasticity that encompasses the niches of virtually all other turkey taxa. The other Meleagris taxa appear to be in effect stenoics, as most of them are susceptible to temperature and precipitation variables. We therefore raise the question of whether the Mexican turkey population is indeed a product of early interaction with human cultures, that later expanded and hybridized with the other subspecies as a result of trade traffic and free-range living in towns. Another element to highlight is the temporal and geographical gaps that exist between the earlier records and the later appearance of the wild turkey in the middle preclassic (1200–400 AD) in localities of central Mexico that represent the first complex societies. Although it is 7
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unknown when it reached the Basin of Mexico, it is relevant that in the earliest prehistoric localities of this geographical area (ca. 4500 years BP) there is no record of the wild turkey (Corona-M., 2009; 2013b). Therefore, it is possible that the austral distribution of this species came later and was influenced by human activities. The models presented provide a proxy for understanding the natural distribution of the genus Meleagris, and later modifications as a result of human actions, in more detail. These models offer a promising perspective for the study of human–animal interactions, allowing us to retrieve information that has previously been difficult to extract from both palaeontological and archaeozoological studies.
Kampichler, C., Calmé, S., Weissenberger, H., Arriaga-Weiss, S.L., 2010. Indication of a species in an extinction vortex: the ocellated Turkey on the Yucatan peninsula, Mexico. Acta Oecol. 36, 561–568. https://doi.org/10.1016/j.actao.2010.08.004. Kraft, K.H., Brown, C.H., Nabhan, G.P., Luedeling, E., Luna Ruiz, J. de J., Coppens d'Eeckenbrugge, G., Hijmans, R.J., Gepts, P., 2014. Multiple lines of evidence for the origin of domesticated chili pepper, Capsicum annuum, in Mexico. Proc. Natl. Acad. Sci. U.S.A. 111, 6165–6170. https://doi.org/10.1073/pnas.1308933111. Larson, G., Piperno, D.R., Allaby, R.G., Purugganan, M.D., Andersson, L., Arroyo-Kalin, M., Barton, L., Climer Vigueira, C., Denham, T., Dobney, K., Doust, A.N., Gepts, P., Gilbert, M.T.P., Gremillion, K.J., Lucas, L., Lukens, L., Marshall, F.B., Olsen, K.M., Pires, J.C., Richerson, P.J., Rubio de Casas, R., Sanjur, O.I., Thomas, M.G., Fuller, D.Q., 2014. Current perspectives and the future of domestication studies. Proc. Natl. Acad. Sci. Unit. States Am. 111, 6139–6146. https://doi.org/10.1073/pnas. 1323964111. Manin, A., Corona-M, E., Alexander, M., Craig, A., Thornton, E.K., Yang, D.Y., Richards, M., Speller, C.F., 2018. Diversity of management strategies in Mesoamerican turkeys: archaeological, isotopic and genetic evidence. Roy. Soc. Open Sci. 5, 171613. https:// doi.org/10.1098/rsos.171613. Martínez-Lira, P., Corona, -M.E., 2016. Possible co-existence of two species of genus Meleagris at Monte Albán, Oaxaca. J. Archaeol. Sci.: Report 10, 632–639. https://doi. org/10.1016/j.jasrep.2016.07.028. Mock, K., Theimer, T., Rhodes, O., Greenberg, D., Keim, P., 2002. Genetic variation across the historical range of the wild Turkey (\emph{Meleagris gallopavo}). Mol. Ecol. 11, 643–657. Navarro-Siguenza, A.G., Peterson, A.T., 2007. Mapas de las aves de Mexico basados en distribución potencial. Museo de Zoología, Facultad de Ciencias, UNAM y University of Kansas Museum of Natural History Available at: http://www.conabio.gob.mx/ informacion/gis/. http://www.conabio.gob.mx/informacion/gis/ [WWW Document]. URL. Padilla-Jacobo, G., Cano-Camacho, H., López-Zavala, R., Cornejo-Pérez, M.E., ZavalaPáramo, M.G., 2018. Evolutionary history of Mexican domesticated and wild Meleagris gallopavo. Genet. Sel. Evol. 50, 19. https://doi.org/10.1186/s12711-0180388-8. Phillips, S.J., Anderson, R.P., Schapire, R.E., 2006. Maximum entropy modeling of species geographic distributions. Ecol. Model. 190, 231–259. https://doi.org/10.1016/j. ecolmodel.2005.03.026. Phillips, S.J., Anderson, R.P., Dudík, M., Schapire, R.E., Blair, M.E., 2017. Opening the black box: an open-source release of Maxent. Ecography 40, 887–893. https://doi. org/10.1111/ecog.03049. QDC Team, 2018. QGIS Geographic Information System. Open Source Geospatial Foundation Project. Ramos-Madrigal, J., Smith, B.D., Moreno-Mayar, J.V., Gopalakrishnan, S., Ross-Ibarra, J., Gilbert, M.T.P., Wales, N., 2016. Genome sequence of a 5,310-year-old maize cob provides insights into the early stages of maize domestication. Curr. Biol. 26, 3195–3201. https://doi.org/10.1016/j.cub.2016.09.036. Sexton, J.P., Montiel, J., Shay, J.E., Stephens, M.R., Slatyer, R.A., 2017. Evolution of ecological niche breadth. Annu. Rev. Ecol. Evol. Syst. 48https://doi.org/10.1146/ annurev-ecolsys-110316-023003. annurev-ecolsys-110316-023003. Speller, C.F., Yang, D.Y., 2015. Identifying the sex of archaeological Turkey remains using ancient DNA techniques. J. Archaeol. Sci.: Report 10, 520–525. https://doi.org/10. 1016/j.jasrep.2016.05.049. Speller, C.F., Kemp, B.M., Wyatt, S.D., Monroe, C., Lipe, W.D., Arndt, U.M., Yang, D.Y., 2010. Ancient mitochondrial DNA analysis reveals complexity of indigenous North American Turkey domestication. Proc. Natl. Acad. Sci. U.S.A. 107, 2807–2812. https://doi.org/10.1073/pnas.0909724107. Steadman, D.W., 1980. A review of the osteology and paleontology of Turkeys (Aves: Meleagridinae). Los Angeles County Museum of Natural History. Contrib. Sci. 330, 131–207 No. 330. Thornton, E., Emery, K.F., Speller, C., 2016. Ancient Maya Turkey husbandry: testing theories through stable isotope analysis. J. Archaeol. Sci.: Report 10, 584–595. https://doi.org/10.1016/j.jasrep.2016.05.011. Thornton, E.K., Emery, K.F., Steadman, D.W., Speller, C., Matheny, R., Yang, D., 2012. Earliest Mexican Turkeys (Meleagris gallopavo) in the Maya region: implications for pre-hispanic animal trade and the timing of Turkey domestication. PloS One 7. https://doi.org/10.1371/journal.pone.0042630. Varela, S., Lima-Ribeiro, M.S., Terribile, L.C., 2015. A short guide to the climatic variables of the last glacial maximum for biogeographers. PloS One 10, 1–15. https://doi.org/ 10.1371/journal.pone.0129037. Vigne, J.-D., 2015. Early domestication and farming: what should we know or do for a better understanding? Anthropozoologica 50, 123–150. https://doi.org/10.5252/ az2015n2a5. Zeder, M.A., 2017. Domestication as a model system for the extended evolutionary synthesis. Interface Focus 7.
Acknowledgements To INAH for funding project 4998: “Estudios paleobiológicos de Morelos y la Cuenca del Balsas”; to CONACYT for the grant A1-S-33096: “Estrategias para el uso y manejo de la fauna en Mesoamérica prehispánica”. To Aurelie Manin and Camilla Speller for the kind contributions to this shared interest. To Joaquin Arroyo Cabrales and the “Seminario Relaciones Hombre-Fauna” (INAH) to give space, coffee, and cookies for the discussions. To the reviewers, their comments help to improve the manuscript. To Stephen Daniel, UBC Anthropology/ Laboratory of Archaeology, PhD student, and to Eva Fairnell for their great work in the edition of grammar and style. To the editors of this volume promoted by the ICAZ Bird Working Group for their kind invitation. References Carrillo-Bastos, A., Islebe, G.A., Torrescano-Valle, N., González, N.E., 2010. Holocene vegetation and climate history of central quintana roo, yucatán península, Mexico. Rev. Palaeobot. Palynol. 160, 189–196. https://doi.org/10.1016/j.revpalbo.2010.02. 013. Corona-M, E., 2002. Las aves en la historia natural novohispana. Instituto Nacional de Antropología e Historia, Mexico. Corona-M, E., 2009. Las Aves en el Cenozoico tardío de Mexico, 1a. ed. Servicio de Publicaciones de la Universidad Autónoma de Madrid, Madrid. Corona-M, E., 2013a. Birds of the Pre-hispanic domestic spheres of Central Mexico. In: Lapham, H. a, Feinman, G.M., Nicholas, L.M. (Eds.), The Archaeology of Mesoamerican Animals. Lockwood Press, Atlanta, pp. 153–190. Corona-M, E., 2013b. Restos prehispánicos de guajolote en Mexico. In: Vidas, A.A., Latsanopoulos, N., Pitrou, P. (Eds.), El Guajolote En Mesoamérica. Enfoques Arqueológicos, Etnohistóricos y Antropológicos. CNRS, Paris. Durán García, R., García Contreras, G., 2010. Distribución espacial de la vegetación. In: Durán-García, R., Méndez-González, M.E. (Eds.), Biodiversidad y Desarrollo Humano En Yucatán. CICY, PPD-FMAM, CONABIO. SEDUMA, Mérida, pp. 131–135. García-Roselló, E., Guisande, C., González–Vilas, L., González–Dacosta, J., Heine, J., Pérez–Costas, E., Lobo, J.M., 2019. A simple method to estimate the probable distribution of species. Ecography ecog, 04563. https://doi.org/10.1111/ecog.04563. Gaut, B.S., 2014. The complex domestication history of the common bean. Nat. Genet. 46, 663–664. https://doi.org/10.1038/ng.3017. Gill, J.L., 2014. Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytologist 1163–1169. https://doi.org/10.1111/nph.12576. Gill, J.L., Williams, J.W., Jackson, S.T., Lininger, K.B., Robinson, G.S., 2014. Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326, 1100–1103. Guisan, A., Thuiller, W., 2005. Predicting species distribution: offering more than simple habitat models. Ecol. Lett. 8, 993–1009. https://doi.org/10.1111/j.1461-0248.2005. 00792.x. Howell, S.N.G., Webb, S., 1995. A Guide to the Birds of Mexico and Northern Central America. Oxford University Press. Johnson, R., 2018. Global Turkey meat market: key findings and insights [WWW document]. The poultry site. URL. https://thepoultrysite.com/news/2018/05/globalturkey-meat-market-key-findings-and-insights, Accessed date: 22 May 2019.
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Quaternary International journal homepage: www.elsevier.com/locate/quaint
Modelling the prehistoric geographical distribution of the genus Meleagris Eduardo Corona-Ma,∗, José Alberto Cruz Silvab a
Instituto Nacional de Antropología e Historia, Centro INAH Morelos, Matamoros 14, Col. Acapantzingo, Cuernavaca, 62440, Mexico Benemérita Universidad Autónoma de Puebla. Laboratorio de Paleontología, Facultad de Ciencias Biológicas, Blvd. Valsequillo y Av. San Claudio, 112 A, Ciudad Universitaria, Col. Jardines de San Manuel, Puebla, 72570, Mexico
b
ARTICLE INFO
ABSTRACT
Keywords: Wild Turkey Meleagris Biogeography Mexico Late Pleistocene Domestication
Studies of the domestication of animals in the Americas suggest strong relationships between humans and a large number of animal species, with the application of many management strategies. Two species of the endemic pheasant genus Meleagris live in America: the wild turkey (Meleagris gallopavo), culturally the most well-known species, with a natural distribution from North America to central Mexico; and the ocellated turkey (Meleagris ocellata), endemic to the Yucatan Peninsula. However, the cultural exchange of both species, which began with the first sedentary human societies, has obscured the natural distributions of both species in central and southern Mexico. We have modelled the geographical distribution of both species based on the amplitude of the ecological niche, a concept that facilitates our understanding of biological adaptations. The models use temperature, precipitation and current distribution data to project back to the late Pleistocene. Three main inferences can be derived from our models. First, during the late Pleistocene both species of Meleagris experienced a reduction and drastic change in their geographical distribution. Second, the speciation events of the genus Meleagris occurred before the late Pleistocene. Third, the subspecies Meleagris gallopavo gallopavo displays the highest niche amplitude, spanning all other M. gallopavo subspecies, suggesting that it could be a product of cultural management.
1. Introduction Mexico is a country with high biological diversity and a large number of endemic species: the 1097 bird species in Mexico represent about 10% of bird species globally (Howell and Webb, 1995). Undoubtedly, this abundance fostered an intense relationship between the ancient cultures of Mexico and birds. For Mesoamerica, particularly in central Mexico, 360 bird species are known, of which 223 have more than one recorded use. In other words, 20% of the overall Mexican bird species count, and more than 60% of the bird species from central Mexico alone, were used culturally in the transition from late prehispanic to early Colonial times, in 16th century (Corona-M., 2002; 2013a). In recent years, the issue of species domestication by prehispanic cultures in America has resurfaced, introducing debates about the chronology, original distribution of wild species, and changes arising from human influence. Examples of plants under discussion include corn, beans and chilli (Gaut, 2014; Kraft et al., 2014; Ramos-Madrigal et al., 2016). An example from animals includes an intensification of research into turkey species (Meleagris spp.) (Mock et al., 2002; Speller
∗
et al., 2010; Corona-M., 2013b; Thornton et al., 2016; Manin et al., 2018; Padilla-Jacobo et al., 2018). Recent archaeozoological findings have shown an early trade in these species in preclassic Mesoamerica (Thornton et al., 2012; Martínez-Lira and Corona-M., 2016; Manin et al., 2018), producing several migratory paths influenced by human groups. This early trade marked the beginning of the dispersal of the wild turkey (Meleagris gallopavo) across practically the whole world. Currently, the leading agro-industrial producers of turkey are the United States, Brazil, Germany and France, representing 66% of the global turkey meat output, while in Mexico the turkey represents barely 2% of national meat production (Johnson, 2018). The wild turkey is one of the most used birds in the global diet, yet we know little detail about its diachronic and spatial dispersal. Current analyses of ancient and modern DNA, stable isotopes and radiocarbon dating provide new data that can be used to help explain the various stages of animal domestication. These methodologies also provide us with an insight into the diversity of strategies that together form the continuous process of domestication, ranging from the management of wild species, through methods of extracting offspring,
Corresponding author. E-mail address: [email protected] (E. Corona-M).
https://doi.org/10.1016/j.quaint.2020.03.053 Received 1 July 2019; Received in revised form 24 March 2020; Accepted 25 March 2020 1040-6182/ © 2020 Elsevier Ltd and INQUA. All rights reserved.
Please cite this article as: Eduardo Corona-M and José Alberto Cruz Silva, Quaternary International, https://doi.org/10.1016/j.quaint.2020.03.053
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Fig. 1. Comparative of current distribution of Meleagris species and subspecies. A) Current distribution of the turkey species Meleagris gallopavo (diagonal lines) and Meleagris ocellata (white area) (data from CONABIO, modified from Navarro and Peterson, 2007). B) Model of potential current distribution of the turkey species M. gallopavo (diagonal lines) and M. ocellata (white area), based on data of this study. C) Current records for M. gallopavo (white triangles) and M. ocellata (white circles), D) Current records for subspecies of M. gallopavo including M. g. gallopavo (circle), M. g. intermedia (triangle), M. g. merriami (cross), M. g. mexicana (square), M. g. silvestris (diamonds) and M. g. osceola (star). Maps 1C and 1D, see material and methods section. D.
captivity and taming, to the production of particular lineages of specific interest to human groups. Differences in these strategies may be associated with the availability of specific animal populations or subpopulations, resulting in the same species displaying different chronologies and domestication events, as has been observed in several ‘traditional’ domestic species, such as horses, dogs and cats (Larson et al., 2014; Vigne, 2015; Zeder, 2017). Animal domestication in Mesoamerica is an understudied subject, and addressing it through a particular case study will serve as a model that could be expanded to other animal groups widely used in prehispanic cultures, such as dogs, deer, rabbits and hares. Seeking to understand wildlife management in past Mesoamerican societies, we have therefore used turkeys as such a case study. The turkey is an endemic American pheasant that includes two species from the genus Meleagris: the wild turkey (Meleagris gallopavo), which is distributed naturally from North America to central Mexico; and the ocellated turkey (Meleagris ocellata), restricted to the Yucatan Peninsula and scarcely known beyond its current location in natural environments and even within its original geographical distribution (Corona-M., 2013b; Manin et al., 2018) (Fig. 1). The wild turkey has received considerable attention in archaeological studies because of its wide geographical distribution in association with diverse American cultures. The oldest specimens of wild turkey in Mexico are found in late Pleistocene contexts on the Mexican Plateau, while the ocellated turkey does not have any Pleistocene records (Corona-M., 2009). Little is known about its speciation process. In the last ten years, significant advances have been made in the development of algorithms that allow modelling of the ecological niche of a species based on a variety of conditions, such as temperature, climate, diversity of foods and range of habitats that a species could inhabit. Recent applications include identifying changes in biogeographical ranges in response to climate change, enhancing our
understanding of biological adaptations (Sexton et al., 2017). Ecological modelling enables quantification of the ecological niche of particular species, and evaluation of the effect of climatic changes and deforestation on biodiversity. However, its most frequent application is modelling the geographical distribution of a particular taxon (Guisan and Thuiller, 2005). This study provides models for the geographical distribution of both species of Meleagris and the subspecies of M. gallopavo in Mexico, based on the amplitude of the ecological niche using temperature, precipitation and current distribution data. We followed a two-step process: first, we obtained current distribution data for the study taxa; second, we factored in the influence of climatic variables on the geographical distribution. Based on this information, models for probable late Pleistocene distributions were then proposed. 2. Material and methods Presence records were obtained from the databases of the Comisión Nacional para el Conocimiento y Uso de la Biodiversidad (www. conabio.gob.mx) (Fig. 1A), Global Biodiversity Information Facility (www.gbif.org) and Integrated Digitized Biocollections (www.idigbio. org) for Meleagris ocellata, and for Meleagris gallopavo and its subspecies (M. g. gallopavo, M. g. intermedia, M. g. merriami, M. g. mexicana, M. g. osceola and M. g. silvestris). Records were reviewed and included only if they were supported by specimens in a scientific collection; sightings only were excluded. These were analysed with QGIS (QDC Team, 2018) and validated using the natural distribution of turkeys indicated by the databases and published sources (Fig. 1B) (Steadman, 1980; Speller et al., 2010). The two-step process of the analysis excluded records of extinct or palaeontological species because they did not have associated reliable climatic records or their phylogenetic relationships were uncertain. However, any future 2
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analysis could factor in those effects. For the subspecies South Mexican turkey (M. g. gallopavo), because of the uncertainty of its natural distribution, the records used had to match two conditions: located in central Mexico, and with specimens in scientific collections identified or referred to as wild, i.e. specimens without evidence of human management. This approach led to the inclusion of fewer records but increased the reliability of the results. The presence records and climatic variables were analysed using Maxent 3.4.0 (Phillips et al., 2006, 2017). The basis of this program is the concept of maximum entropy, in order to make predictions from incomplete information. Maxent estimates the most uniform distribution throughout the study area with the restriction that the expected value for each environmental variable agrees with its empirical average, i.e. the average values for the occurrence data set (Phillips et al., 2006, 2017). Five potential distribution models were made with bootstrapping for each of the taxa, and the one with the best performance was selected. The parameters used were random test percentage = 30% and regularization multiplier = 1, discarding the clamping option. The model fit estimator area under the curve (AUC) was chosen, using the highest value, because it is not threshold dependent, unlike other evaluation metrics such as sensitivity, specificity and true skill statistics (TSS), and is therefore considered a more reliable metric for comparing results from different ecological niche models (García–Roselló et al., 2019). The resulting models were analysed further with QGIS, to obtain binary values for presence (1) and absence (0) for each of the species and subspecies, using the ten percentile training presence as a threshold. The ecological niche models revealed the contribution of climatic variables, such as the values of average annual temperature and annual precipitation, to the potential distribution of each taxon. The Last Glacial Maximum (LGM) models (ca. 21,000 years BP) were based on projections of the presence records and the climatic variables available in Worldclim version 1.4 (www.worldclim.com), and also on the MIROC-ESM global climate model (www.ecoclimate.org/ downloads). Comparisons between ancient and current potential distributions provide us with an understanding of the geographical changes from the LGM onwards (Varela et al., 2015).
Table 1 The relative contribution (%) of the bioclimatic variables used in the ecological niche models for Meleagris gallopavo and Meleagris ocellata. Bold values indicate the variables with the highest importance for the modelled potential distributions. Climatic variable
M. gallopavo
M. ocellata
Bio1: Annual mean temperature Bio2: Mean diurnal range Bio3: Isothermality Bio4: Temperature seasonality Bio5: Max temperature of the warmest month Bio6: Min temperature of the coldest month Bio7: Temperature annual range Bio8: Mean temperature of wettest quarter Bio9: Mean temperature of the driest quarter Bio10: Mean temperature of warmest quarter Bio11: Mean temperature of coldest quarter Bio12: Annual precipitation Bio13: Precipitation of wettest month Bio14: Precipitation of driest month Bio15: Precipitation seasonality Bio16: Precipitation of wettest quarter Bio17: Precipitation of driest quarter Bio18: Precipitation of warmest quarter Bio19: Precipitation of coldest quarter
0.2 1.8 0.1 7.0 13.2 44.5 2.8 3.0 6.2 1.2 1.4 0.3 9.9 0.3 0.9 0.0 0.1 1.6 5.5
1.4 0.3 24.2 19.2 0.1 26.1 9.4 1.6 0.7 0.2 9.1 0.0 1.5 4.2 0.1 0.2 0.8 0.3 0.6
Bio6, Bio7 and Bio11 variables suggested a more stable environment, very similar to the restricted habitats of humid forests and brushy woodlands that occur in the Yucatan Peninsula (Howell and Webb, 1995). However, despite these differences in the climatic conditions, both species shared the variable related to the minimum temperature of the coldest month (Bio6). Remarkably, of the climatic variables that were most influential in constructing the models for both species, only precipitation was of relative importance geographically for the wild turkey. To observe any differences between the climatic niches of each species, the values for annual average temperature and annual precipitation were extracted from the potential distribution. For average annual temperature, the climatic niche of the wild turkey was broader, ranging from 1.5 °C to 25 °C, while for the ocellated turkey it was narrower, ranging from 22.5 °C to 26.6 °C. (Fig. 2). It is important to note that the overlap in average annual temperature values for the two species was very small. The breadth of the climatic niche was wider for the wild turkey, as indicated by the annual average temperature. However, the overlap of annual precipitation values was wider between the two species (Fig. 2). For annual precipitation, the wild turkey had a higher tolerance to drier conditions (less than 700 mm) than the ocellated turkey, which had a higher tolerance of more humid environments.
3. Results and discussion We obtained 621 unique records for M. gallopavo and 677 records for M. ocellata (Fig. 1C). For the subspecies of M. gallopavo, the records numbered M. g. gallopavo (10), M. g. intermedia (97), M. g. merriami (61), M. g. mexicana (35), M. g. osceola (37) and M. g. silvestris (273) (Fig. 1D). 3.1. Distribution and climatic niche of Meleagris species The models for the current potential distribution of M. gallopavo and M. ocellata did not overlap (Fig. 1A and B). The areas were smaller than those shown in Fig. 1A, which is the distribution as determined by the Commission for the Use and Management of Biodiversity (CONABIO in Spanish) (Navarro-Siguenza and Peterson, 2007). These differences may have arisen because our database did not include sighting-only records, which could lead to geographical over-representation. However, if this distribution provides a better fit to the environmental conditions that determine the niche, then this reduction in habitat may illustrate the current Anthropocene conditions better, such that we are observing habitat fragmentation and smaller areas than previously published. The climatic variables making the most significant contribution to the current geographical distribution models differed between the two species (Table 1). For the wild turkey, a combination of Bio5, Bio 6 and Bio13 variables suggested tolerance of a broad range of temperature and precipitation, which explained its wide distributional range in North America. For the ocellated turkey, the combination of Bio3, Bio4,
3.2. Distribution and climatic niche of Meleagris gallopavo subspecies Ecological niche models for the distribution of each subspecies of the wild turkey showed a clear separation for most of them, suggesting that climatic conditions had the most influence on their geographical distribution (Fig. 3A). However, there are two exceptions worthy of discussion. First, the Gould turkey (M. g. mexicana) has a potential distribution that falls within that of the Merriam turkey (M. g. merriami) (Fig. 3A), suggesting a close relationship between them. A possible explanation for this is provided by Manin et al. (2018), who show that these two subspecies are very close phylogenetically and share the H2 haplotype, which in biogeographical terms also suggests a close interaction between these subspecies. This raises the question of whether the geographical distribution encompassing both subspecies is a product of trade and management by ancient human cultures in this area. The management of the Gould turkey in two cultural areas, Mesoamerica and Oasisamerica, is of 3
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Table 2 The relative contribution (%) of the bioclimatic variables used in the ecological niche models for the Meleagris gallopavo subspecies. Bold values indicate the variables with the highest importance for the modelled potential distributions. See Table 1 for the definitions of the bioclimatic variables. Climatic variable
M. g. gallopavo
M. g. intermedia
M. g. merriami
M. g. mexicana
M. g. osceola
M. g. silvestris
Bio1 Bio2 Bio3 Bio4 Bio5 Bio6 Bio7 Bio8 Bio9 Bio10 Bio11 Bio12 Bio13 Bio14 Bio15 Bio16 Bio17 Bio18 Bio19
22.9 0.1 1.4 0.3 0.0 43.4 1.4 10.2 0.1 0.0 13.7 0.2 0.0 0.0 0.0 0.0 0.0 0.7 5.6
0.4 1.0 0.0 5.2 0.4 15.2 1.4 0.4 10.3 36.7 10.7 0.2 0.0 5.6 8.4 0.0 0.9 2.4 0.8
5.5 12.6 48.4 6.0 3.1 0.0 0.3 2.7 0.8 4.1 4.6 0.1 2.9 0.8 3.7 0.2 1.6 1.3 1.3
8.1 6.0 35.0 2.3 0.1 6.9 0.4 0.2 0.9 0.2 3.6 0.1 5.3 3.8 11.8 1.2 1.7 6.9 5.7
0.4 0.0 1.7 12.6 0.0 0.3 0.3 11.8 0.2 0.5 0.0 0.0 0.8 5.0 7.2 0.0 0.0 59.1 0.1
1.1 0.2 0.2 4.5 2.4 4.8 0.6 1.6 1.2 17.3 4.6 4.0 0.0 5.6 11.6 0.6 35.6 3.8 0.1
and the Merriami turkey (M. g. merriami). For the rest of the M. gallopavo subspecies, at least one precipitation variable was indicated (Table 2). For the subspecies in eastern North America, the Florida turkey (M. g. osceola) and Eastern turkey (M. g. silvestris), precipitation of the warmest quarter (Bio18) and precipitation of the driest quarter (Bio17), respectively, contributed most to their modelled distributions (Table 2), suggesting a more humid environment. All of these results were consistent with a possible differentiation of climatic niche between the subspecies of M. gallopavo. When extracting the average annual temperature values for each of the subspecies of wild turkey, the Mexican turkey (M. g. gallopavo) presented a broad overlap and encompassed practically all the climatic niches of the rest of the subspecies. This suggests that a high tolerance to different climatic conditions is the product of interactions with humans (Fig. 4). There is a clear differentiation in the amplitude of average annual temperature for the Rio Grande turkey (M. g. intermedia) and Florida turkey (M. g. osceola), because they are located in areas with higher temperatures compared with the rest of the subspecies. For the Merriami (M. g. merriami), Gould (M. g. mexicana) and Eastern (M. g. silvestris) turkeys, extensive overlaps between the average annual temperature values exist (Fig. 4). These three subspecies are located in central North America and reach the east and west coasts of Mexico. The human cultures in those areas interacted significantly with these
Fig. 2. Climatic values of mean annual temperature (° C) and annual precipitation (mm) in geographical ranges of M. gallopavo (dashed line) and M. ocellata (continuous line).
particular interest, but addressing this lies outside the scope of this paper. Second, the other subspecies of interest within a Mesoamerican context is the Rio Grande turkey (M. g. intermedia), with a current distribution extending towards eastern Mexico and the United States but not reaching central Mexico. This model suggests that the expansion of the Rio Grande turkey is the result of trade and cultural traffic. The most unusual and broadest potential distribution is that of the subspecies South Mexican turkey (M. g. gallopavo), which encompasses the distribution of all other subspecies and beyond towards the south (Fig. 3B). Archaeological samples of this subspecies share haplotypes (Hap 1 and Hap 2) and are found in practically all regions of Mexico apart from the north (Manin et al., 2018). This result raises the question of whether the geographical distribution of this subspecies is a product of its management, expanding rapidly because of its association with human cultures. The data suggest that this is a highly probable event, but further phylogeographic research is needed to explore this fully. Regarding the percentage contribution of climatic variables to the ecological niche models for each subspecies (Table 2), temperature variables contributed the most for the Mexican turkey (M. g. gallopavo)
Fig. 3. Distribution of Meleagris gallopavo subspecies. A) M. g. intermedia (front diagonal lines \\), M. g. merriami (vertical lines), M. g. mexicana (white area), M. g. osceola (back diagonal lines///) and M. g. silvestris (horizontal lines). B) M. g. gallopavo (white area). 4
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Fig. 4. Climatic values of mean annual temperature (° C) and annual precipitation (mm) in geographical ranges of. gallopavo subspecies including M. g. gallopavo (continuous black line), M. g. intermedia (dotted grey line), M. g. merriami (continuous grey line), M. g. mexicana (dashed black line), M. g. osceola (dashed grey line) and M. g. silvestris (dotted black line).
three subspecies, and the climatic conditions possibly favoured their management and trade. When examining the data for average annual precipitation, the Mexican turkey shows similar results as for temperature, with this subspecies spanning the curves of practically all other subspecies and indicating a tolerance of more humid environments, including those with more than 800 mm of rainfall (Fig. 4). However, in spite of the overlap in precipitation curves, some differentiation is evident (Fig. 4). The Merriami and Gould turkeys tolerate the driest habitats, which is congruent with their location in the Highlands of North America and Mexico. The Florida and Eastern turkeys prefer the more humid environments in eastern North America, while the Rio Grande turkey tolerates intermediate values of average rainfall and its distributional range falls between those of the Florida and Eastern turkeys (Figs. 3 and 4).
for North America and Mexico (Steadman, 1980; Corona-M., 2009). A disjunct population is modelled in the southeastern United States, where a continuum might have been expected, as is also the case today. Two hypotheses could explain this. First, a population covering a greater distributional range before the LGM was split towards the end of this period, perhaps as a result of changes in vegetation, as the models indicate that some populations of wild turkey are susceptible to climatic variables. Second, in the early Holocene, the separated wild turkey populations were able to rejoin across the original distributional area, but with distinctive haplotypes, as suggested by the populations of Florida and Eastern turkeys. This raises the possibility that both subspecies are the product of changes in the early Holocene, which is certainly an issue for further research. For the ocellated turkey (M. ocellata), the model suggests its presence in the east and south of the Yucatan Peninsula. If we consider the vegetation extant before intensive human use, this is an area of humid forests, while dry forest is located to the northwest of the peninsula (Durán García and García Contreras, 2010). A hypothesis therefore arises of an original association of the ocellated turkey with humid vegetation. In that case, the areas indicated by the model also suggest a reduction in distribution in eastern Yucatan Peninsula, with a shift towards the south and a division into two areas that comprise the east of the Yucatan Peninsula and the flood zone of the state of Tabasco, where currently the species is not found naturally. The possible presence of a separate population could be explained by a reduction in the range of a
3.3. A late Pleistocene models of Meleagris species and subspecies The ecological niche distributional models were projected to the late Pleistocene, in particular to the LGM (ca. 21,000 years BP). For the wild turkey (M. gallopavo) the model shows a narrower distributional range than models for the present-day. The distribution indicates the presence of wild turkey in the Highlands of North America and Mexico, but it does not reach central Mexico (Fig. 5). This matches the distribution of most of the late Pleistocene records for the genus Meleagris 5
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Fig. 5. Potential distribution inferred for the late Pleistocene (~21,000 years BP) in the Last Glacial Maximum. Pleistocene distributions of M. gallopavo (front diagonal lines \\) and M. ocellata (vertical lines) compared to the current distributions of M. gallopavo (back diagonal lines///) and M. ocellata (horizontal lines).
large ancient population that originally covered the whole area, and, near the LGM, an extirpation of the population in the Tabasco area. This model is congruent with evidence provided by pollen studies that shows climatic and dynamic vegetational changes from the late Pleistocene to the Holocene (Gill, 2014; Gill et al., 2014). In some areas of the Yucatan Peninsula, changes from medium to low stature forest have been documented by 7500 cal years BP, and later changes from moist to drier conditions (Carrillo-Bastos et al., 2010). Finally, throughout the Holocene, the surviving population of ocellated turkey consolidated its presence and expanded to cover all types of vegetation across the Yucatan Peninsula, i.e. tropical deciduous forest, humid forest and a later humanized habitat known as milpa, where it is found currently (Howell and Webb, 1995). However, in the last few decades, with a reduction in their range because of the growth of the human population, the species is facing a severe extinction risk (Kampichler et al., 2010). The habitat changes of the ocellated turkey therefore need further urgent review. Another question arising is when the original population of the genus Meleagris split into the current two species. Any hypothesis needs to include the ancient and large turkey population, from the early Pleistocene or earlier, that inhabited the north of America and the east of Mexico, including the Yucatan Peninsula, which may have been associated with brushy woodland and temperate woods. Across different episodes of climatic and vegetational change, this population suffered fragmentation and local extinctions, the data from our model updating Steadman's (1980) proposal. The origin of ocellated turkey as a species could therefore be located in the Blancan or Irvingtonian time periods. Comparing the late Pleistocene models for wild turkey subspecies show interesting distributional changes. The most remarkable is the Mexican turkey subspecies (M. g. gallopavo), which shows an extensive distributional range, from southern Mexico through to the Panama Bridge and northern part of South America, while to the west it includes the Caribbean (Fig. 6E). This is an unusual result as no record of any wild turkey exists in these areas from that time. This model may therefore be reinforcing the hypothesis given above that the Mexican turkey population is a product of cultural management. Another compelling case is the Florida turkey (M. g. osceola), for which, after modelling, there does not appear to have been optimal climatic conditions during the Pleistocene. It is possible that this
subspecies split from ancient Eastern (M. g. silvestris) or Rio Grande (M. g. intermedia) turkey populations that expanded to Florida during the early Holocene (Fig. 6A and D). The first option is consistent with the evidence provided by Mock (2002). The distribution of the Rio Grande turkey shows a southern displacement in its present range compared with the ideal climatic conditions for this subspecies in Florida (Fig. 6A). The range of the Merriami turkey (M. g. merriami) has changed, losing areas in which it is currently present, but also expanding in eastern America, particularly in the western United States and in Mexico from the northwest and to central Mexico in the Highlands (Fig. 6B). Finally, the model for the Gould turkey (M. g. mexicana) suggests a broad area of distribution in southern North America and north of Mexico in the Highlands (Fig. 6C). Both the present and Pleistocene populations of the Merriami turkey overlap with the range of Gould turkey, and it is probable that before the LGM they were neighbouring populations. An expansion of the Merriami turkey could have caused the overlap. It is interesting that these two subspecies are associated with management processes in Oasisamerica, while the Gould turkey is also associated with cultures in Mesoamerica, as illustrated by Manin et al. (2018). 4. Final considerations The wild turkey population in the LGM model inhabited the southern part of North America. It is probable that the influence of climatic events near the LGM fragmented the population on an east–west axis, located in the Highlands and limited by the Sierras Madre in Mexico. This phenomenon has been observed in several species of birds (Corona-M., 2009) and is illustrated by the models for subspecies of wild turkey here discussed. The evidence also suggests that the Meleagris speciation events occurred before the LGM. Based on the palaeontological record, the genus can be traced back to the Blancan or Irvingtonian time periods, during which many phenomena that changed the configuration of American biodiversity have been detected, such as the Great American Biotic Exchange (Corona-M., 2009). These issues should therefore be part of further modelling. The models obtained for the two species, for both the present and 6
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Fig. 6. Potential current distribution (back diagonal lines///) and inferred distribution for the late Pleistocene (~21,000 years BP) in the Last Glacial Maximum (front diagonal lines \\) of the subspecies of M. gallopavo. A) M. g. intermedia, B) M. g. merriami, C) M. g. mexicana, D) M. g. silvestris, E) M. g. gallopavo, and F) M. g. osceola shows only the current distribution since the Pleistocene does not have optimal climatic conditions for an ecological niche model.
the LGM, allow us to confirm the hypothesis that the natural distribution of the wild turkey is in the Highlands of Mexico and North America, where a temperate climate predominates, associated with the Nearctic region. Their southern limit appears to be in the Mexican Neovolcanic Axis (Corona-M., 2009), and the distributional range of wild turkey in all models, current and Pleistocene, extends to this southern limit. This suggests that the records of wild turkey in the preclassic of central and southern Mexico are a product of trade and management (Thornton et al., 2012; Corona-M., 2013b; Martínez-Lira and Corona-M., 2016). It is interesting to note the dynamics of expansion and shrinkage in the distribution of the species and subspecies of Meleagris during the Pleistocene–Holocene transition. Our modelling introduces the LGM as a boundary for discussing a number of hypotheses about ancient distributions and splits of turkey populations. In particular, these models show considerable congruence with genetic evidence (Mock et al., 2002; Speller et al., 2010; Speller and Yang, 2015; Manin et al., 2018) and suggest that the distributional ranges are
a product of climatic changes from the late Pleistocene (LGM) onwards. The subspecies most likely to have interacted with early cultures are the Rio Grande (M. g. intermedia), Merriami (M. g. merriami) and Gould (M. g. mexicana) turkeys, as also indicated by the archaeogenetic record (Manin et al., 2018). The Mexican turkey subspecies (M. g. gallopavo) appears to be a eurioic population, with high environmental plasticity that encompasses the niches of virtually all other turkey taxa. The other Meleagris taxa appear to be in effect stenoics, as most of them are susceptible to temperature and precipitation variables. We therefore raise the question of whether the Mexican turkey population is indeed a product of early interaction with human cultures, that later expanded and hybridized with the other subspecies as a result of trade traffic and free-range living in towns. Another element to highlight is the temporal and geographical gaps that exist between the earlier records and the later appearance of the wild turkey in the middle preclassic (1200–400 AD) in localities of central Mexico that represent the first complex societies. Although it is 7
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unknown when it reached the Basin of Mexico, it is relevant that in the earliest prehistoric localities of this geographical area (ca. 4500 years BP) there is no record of the wild turkey (Corona-M., 2009; 2013b). Therefore, it is possible that the austral distribution of this species came later and was influenced by human activities. The models presented provide a proxy for understanding the natural distribution of the genus Meleagris, and later modifications as a result of human actions, in more detail. These models offer a promising perspective for the study of human–animal interactions, allowing us to retrieve information that has previously been difficult to extract from both palaeontological and archaeozoological studies.
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Acknowledgements To INAH for funding project 4998: “Estudios paleobiológicos de Morelos y la Cuenca del Balsas”; to CONACYT for the grant A1-S-33096: “Estrategias para el uso y manejo de la fauna en Mesoamérica prehispánica”. To Aurelie Manin and Camilla Speller for the kind contributions to this shared interest. To Joaquin Arroyo Cabrales and the “Seminario Relaciones Hombre-Fauna” (INAH) to give space, coffee, and cookies for the discussions. To the reviewers, their comments help to improve the manuscript. To Stephen Daniel, UBC Anthropology/ Laboratory of Archaeology, PhD student, and to Eva Fairnell for their great work in the edition of grammar and style. To the editors of this volume promoted by the ICAZ Bird Working Group for their kind invitation. References Carrillo-Bastos, A., Islebe, G.A., Torrescano-Valle, N., González, N.E., 2010. Holocene vegetation and climate history of central quintana roo, yucatán península, Mexico. Rev. Palaeobot. Palynol. 160, 189–196. https://doi.org/10.1016/j.revpalbo.2010.02. 013. Corona-M, E., 2002. Las aves en la historia natural novohispana. Instituto Nacional de Antropología e Historia, Mexico. Corona-M, E., 2009. Las Aves en el Cenozoico tardío de Mexico, 1a. ed. Servicio de Publicaciones de la Universidad Autónoma de Madrid, Madrid. Corona-M, E., 2013a. Birds of the Pre-hispanic domestic spheres of Central Mexico. In: Lapham, H. a, Feinman, G.M., Nicholas, L.M. (Eds.), The Archaeology of Mesoamerican Animals. Lockwood Press, Atlanta, pp. 153–190. Corona-M, E., 2013b. Restos prehispánicos de guajolote en Mexico. In: Vidas, A.A., Latsanopoulos, N., Pitrou, P. (Eds.), El Guajolote En Mesoamérica. Enfoques Arqueológicos, Etnohistóricos y Antropológicos. CNRS, Paris. Durán García, R., García Contreras, G., 2010. Distribución espacial de la vegetación. In: Durán-García, R., Méndez-González, M.E. (Eds.), Biodiversidad y Desarrollo Humano En Yucatán. CICY, PPD-FMAM, CONABIO. SEDUMA, Mérida, pp. 131–135. García-Roselló, E., Guisande, C., González–Vilas, L., González–Dacosta, J., Heine, J., Pérez–Costas, E., Lobo, J.M., 2019. A simple method to estimate the probable distribution of species. Ecography ecog, 04563. https://doi.org/10.1111/ecog.04563. Gaut, B.S., 2014. The complex domestication history of the common bean. Nat. Genet. 46, 663–664. https://doi.org/10.1038/ng.3017. Gill, J.L., 2014. Ecological impacts of the late Quaternary megaherbivore extinctions. New Phytologist 1163–1169. https://doi.org/10.1111/nph.12576. Gill, J.L., Williams, J.W., Jackson, S.T., Lininger, K.B., Robinson, G.S., 2014. Pleistocene megafaunal collapse, novel plant communities, and enhanced fire regimes in North America. Science 326, 1100–1103. Guisan, A., Thuiller, W., 2005. Predicting species distribution: offering more than simple habitat models. Ecol. Lett. 8, 993–1009. https://doi.org/10.1111/j.1461-0248.2005. 00792.x. Howell, S.N.G., Webb, S., 1995. A Guide to the Birds of Mexico and Northern Central America. Oxford University Press. Johnson, R., 2018. Global Turkey meat market: key findings and insights [WWW document]. The poultry site. URL. https://thepoultrysite.com/news/2018/05/globalturkey-meat-market-key-findings-and-insights, Accessed date: 22 May 2019.
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