Niche divergence and paleo-distributions of Lutzomyia longipalpis mitochondrial haplogroups (Diptera: Psychodidae)
Introduction
Although allopatric speciation occurs due to geographic barriers that prevent dispersal among diverging populations or lineages (Coyne and Orr, 2004), it could also be driven by ecological variation. Variation may be due to adaptation to alternative niches and/or from the geographic disruption of the optimal ecological niche for a species (vicariance), leading to ecological niche specialization (Moritz et al., 2000; Wiens and Graham, 2005; Warren et al., 2008). Speciation events would occur either due to niche divergence or niche conservation (Hua and Wiens, 2010). Niche conservatism implies that species´ distribution patterns are governed by ancestral climate affinities, resulting in high ecological niche space overlap between related species (Warren et al., 2008). Conversely, niche divergence occurs when the speciation process takes place in an alternative niche to the original occupied, so that sister species are more divergent in their niche space than would be expected by chance (Hua and Wiens, 2010). Ecological niche modelling (ENM) can quantify changes in species´ distributions over time due to climate change, providing a measure of ecological divergence, or the degree of niche conservatism within and among species, or closely-related species (Wiens and Graham, 2005).
Climate change since the Last Glacial Maximum (LGM; 21,000 yrs before the present) and late Pleistocene has been a major driver in shaping current species´ distributions and the diversification of extant species (Avise, 2000). During the Pleistocene, more than 50 glacial/interglacial cycles of varying magnitude were recorded (depending on the region; Benedetto, 2012), which have strongly influenced not only species´ geographic distributions, but also their demography and genetic diversity (Moritz et al., 2000; Hewitt, 2004; Ramírez-Barahona and Eguiarte, 2013). The “refugia” hypothesis, developed for tropical forests of the Neotropical region, proposes that persistent patches despite successive climate and vegetation cycles since the LGM, may be drivers of both expansions and contractions of species distributions’. The latter would also be affected by the reduction, fragmentation, and isolation of forest patches within a background of non-forest vegetation (Haffer and Prance, 2001; de Mello-Martins, 2011; Ramírez-Barahona and Eguiarte, 2013). Speciation would then occur differentially within isolated forest refuges during dry/cool periods (glacials), and in savanna refuges during wet/hot periods (inter-glacials) (Werneck et al., 2011). In general, biogeographic (e.g. orogeny and marine incursion) and geologic (climate oscillation) events that occurred during the late Pliocene-Pleistocene in Central and South America, are considered to have been influential for many species´ diversifications (Arrivillaga et al., 2002; 2003; Conn and Mirabello, 2007).
Lutzomyia longipalpis (Lutz and Neiva) is the most widely studied sandfly in the American continent, and is also the most important vector of Leishmania (Leishmania) infantum Nicolle (synonyms Le. chagasi, Cunha and Chagas), etiologic agent of Visceral Leishmaniasis (VL) (Lainson and Rangel, 2005). There is an estimated 4500 to 6800 new cases of VL annually in Latin America, although most of these occur in Brazil (Alvar et al., 2012). Lutzomyia longipalpis is a complex of species, which has a wide but discontinuous distribution from southeastern Mexico to northern Argentina and Uruguay (Young and Duncan, 1994; Salomón et al., 2011). Mangabeira (1969) was the first to suggest the existence of a Lu. longipalpis´ complex, based on ecological and morphological evidence. Increasing interest in the Lu. longipalpis complex is due to its potential impact on vector capacity and specifically, to female susceptibility to the pathogen, infection rates and pathogen load, female longevity, dispersal capacity, and epidemiological traits (Lanzaro et al., 1993). Evidence for genetic divergence and cryptic speciation exists from reproductive, morphological, isoenzyme, biochemical, and genetic traits (Soto et al., 2001; Arrivillaga et al., 2002; 2003; Hamilton et al., 2005; Pech-May et al., 2018). Mitochondrial genes have been shown to be good molecular markers to analyze genetic diversity, population genetics, molecular taxonomy, phylogeography, and speciation in sandflies from the New and the Old World (Soto et al., 2001; Arrivillaga et al., 2002; Flanley et al., 2018; Pech-May et al., 2018; Rodrigues et al., 2018; Barroso et al., 2020). They are maternally inherited, abundant, with little or no recombination, and are particularly appropriate for recently diverged lineages (Avise, 2000, Avise, 2009). Soto et al. (2001) used the ND4 gene to identify two primary clades (South America and Central America) and four subclades, significantly supported using specimens from Brazil, Central America, and laboratory colony populations from Colombia and Venezuela. Similarly, Arrivillaga et al. (2002; 2003), using the COI, 12S, and 16S genes, also identified four subclades (Laran: Venezuela; cis-Andean: Venezuela, Colombia, northern Brazil; trans-Andean: Venezuela, Colombia, Central America; and Brazilian: Brazil). Despite the above, it is still unclear how many lineages or species belong to the complex, since there is no robust molecular information for some geographic areas and insufficient collections for others, and there is discordant evidence for certain biological traits (e.g. ‘sexual songs’ vs genetic markers). To date, two primary clades and eight haplogroups have been significantly supported across the continent using mitochondrial markers. The results using Bayesian inference strongly support several mutational steps with high posterior probabilities, high pairwise FST and nucleotide divergence, and indicate negligible gene exchange (Pech-May et al., 2018).
Ecological niche expansion of the complete complex in future climate scenarios, has been reported for North and Central America (NCA) (Moo-Llanes et al., 2013), while geographic distribution shifts are projected in the future on a continental scale (Peterson et al., 2017). NCA paleo-distributions for the complex have revealed highly conserved niche (88%) between the LGM and current projections (Moo-Llanes et al., 2019). All previous ENM analyses have analyzed Lu. longipalpis as a single clade, despite genetic structuring summarized above, and discontinuous distributions of both the vector complex and VL incidence in the continent. The aim of the present study was to analyze whether genetic diversification of the Lu. longipalpis complex (based on three mitochondrial genes) is associated with niche divergence, and to explore the historical effect of climate changes on ENM shifts in haplogroup distributions. Current and LGM bioclimatic variables were used to project the ENM for each haplogroup, to quantify geographic area shifts as well as coverage maintained over time, and to estimate ENM divergence between haplogroups.
Section snippets
Database
A database was compiled combining Lu. longipalpis occurrence records from Mexico through Central America (CA), Colombia, Venezuela, Brazil, Argentina, and Paraguay (Valderrama et al., 2011; Moo-Llanes et al., 2013; Peterson et al., 2017; Pech-May et al., 2018). The two primary clades and haplogroups were defined based on the most recent Bayesian inference phylogenetics using three mitochondrial genes: ND4, cyt b and COI (Pech-May et al., 2018; Moya et al., 2020, in press). Several geographic
ENM Parameters
A total of 13,311 candidate models were built with all sets of predictors for all haplogroups or combinations of haplogroups from the complex (Table 1). Bio03 and Bio04 were the variables shared by both major clades of the first scheme. Significant ENM variables for individual haplogroups, or the northern haplogroup combinations, were Bio03 (4 haplogroups), Bio04 (5 haplogroups), Bio06 (5 haplogroups), Bio07 (4 haplogroups), Bio10 (5 haplogroups), Bio12 (3 haplogroups), Bio14 (3 haplogroups),
Discussion
The present study analyzed whether Lu. longipalpis haplogroups genetically diverge maintaining similar ecological niche (conservatism) or by occupying distinct niche (divergence). Shared environmental space was not low between the major northern and southern Lu. longipalpis phylogenetic clades, but it was significantly different indicating niche divergence. Divergent yet overlapping niches between these two major clades are consistent with the high ecological plasticity previously evidenced for
Funding
This work received funding from IDRC # 107577 “Addressing the emergence and dispersion of Leishmaniasis in the border of Argentina, Brazil, Paraguay and Uruguay” to O. D. Salomón and from project CONACyT 261006 to JM Ramsey.
Declaration of Competing Interest
None
CRediT authorship contribution statement
David A. Moo-Llanes: Conceptualization, Formal analysis, Investigation, Writing - original draft, Writing - review & editing. Angélica Pech-May: Conceptualization, Investigation, Writing - original draft, Writing - review & editing. Ana C. Montes de Oca-Aguilar: Formal analysis, Investigation, Writing - original draft, Writing - review & editing. Oscar D. Salomón: Investigation, Writing - review & editing, Funding acquisition. Janine M. Ramsey: Conceptualization, Investigation, Writing -
Acknowledgements
We acknowledge Townsend Peterson for invaluable comments on the manuscript. DAM-L was a doctoral student from Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México (UNAM) and received fellowship #231741 from CONACYT.
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