2 Department of Sciences, Museums Victoria,
Melbourne, VIC, Australia
Abstract
Differences in the geographic scale and depth of phylogeographic
structure across co-distributed taxa can reveal how microevolutionary
processes such as population isolation and persistence drive
diversification. In turn, environmental heterogeneity, species’ traits
and historical biogeographic barriers may influence the potential for
isolation and persistence. Using extensive SNP data and a combination of
population genetic summary statistics and landscape genomic analyses, we
explore predictors of the scale and depth of phylogeographic structure
in co-distributed lizard taxa from the topographically and climatically
complex monsoonal tropics (AMT) of Australia. We first resolve
intraspecific lineages and then test whether genetic divergence across
space within lineages is related to isolation by distance, resistance
and/or environment, and whether these factors differ across genera or
between rock-related versus habitat generalist taxa. We then test
whether microevolutionary processes within lineages explain differences
in the geographic scale and depth of intraspecific phylogeographic
lineages. Results indicate that landscape predictors of phylogeographic
structure differ between taxa. Within lineages, there was prevalent
isolation by distance, but the strength of isolation by distance is
independent of the taxonomic family, habitat specialization and climate.
Isolation by environment is the strongest predictor of landscape-scale
genetic divergence for all taxa, with both temperature and precipitation
acting as limiting factors. The strength of isolation by distance does
not predict the geographic scale of phylogeographic structure. However,
more localized lineages had higher mean individual heterozygosity and
less negative Tajima’s D. This implies that finer-scale phylogeographic
structuring within species is associated with larger and more stable
populations and, hence, persistence.
Keywords
Population structure, gene flow, isolation by distance, geographic
barriers, environmental limitation
Introduction
The immense variety of life forms that we observed today is a result of
the speciation process- and all the factors that promote speciation
initiation. Speciation is an extended process where the potential for
persistence of population isolates is central to whether intraspecific
lineages are ephemeral, or will eventually transition to full species
under the protracted speciation model (Etienne et al., 2012; Rosenblum
et al., 2012). Population isolation and high persistence of isolates
manifests as a strong phylogeographic structure across the range of
species (or parapatric species complexes). It follows that the
phylogeographic structure of taxa depends on how a combination of
species traits (e.g. specialization to spatially patchy habitats),
environmental heterogeneity and biotic interactions (Harvey, Aleixo,
Ribas & Brumfield, 2017; Riginos, Buckley, Blomberg, & Treml, 2014)
influence isolation and/or persistence of populations (Funk et al.,
2005; Oliveira et al., 2018; Pease et al., 2009). Understanding how
genetic differentiation is shaped by environmental heterogeneity and
dispersal limitation can help predict potential for adaptive divergence
(Wang & Bradburd, 2014), in addition to informing how geographical and
climatic barriers influence phylogeographic structure (Li, Huang,
Sukumaran, & Knowles, 2018).
A broad spatial view of the population dynamics associated with species
formation provides a bridge of two largely isolated research approaches
– macro and microevolution (Harvey, Singhal & Rabosky, 2019). While
macroevolution is broadly concerned with rates of speciation and
extinction among groups, microevolutionary processes include intrinsic
dispersal limitation, estimated using isolation by distance (Singhal et
al., 2018; Strien, Holderegger, & Van Heck, 2015; Wright, 1943),
extrinsic dispersal limitation related to the presence, currently or in
the past, of geographic and physiological dispersal barriers (Myers et
al., 2019; Pelletier & Carstens, 2018; Yannic, Hagen, Leugger, Karger
& Pelissier, 2020), and population persistence through past climates
(Bell et al., 2010; Ortego, Gugger, Riordan, & Sork, 2014; Vasconcellos
et al., 2019).
Here we apply landscape genetics methods to a tropical reptile fauna in
which most species have phylogeographic structuring, but with varying
spatial and temporal scales. We explore whether dispersal within
lineages is limited by geographic distance (isolation by distance (IBD);
Wright, 1943), environmental heterogeneity (isolation by environment
(IBE); Wang & Bradburd, 2014), or geographic barriers (isolation by
resistance (IBR); Cushman, McKelvey, Hayden, & Schwartz, 2006; Spear,
Balkenhol, Fortin, McRae, & Scribner, 2010), and how these
relationships vary across rock-restricted vs. habitat-generalist
species, or across genera, representing broader trait variation. We also
test whether phylogeographic structuring is more geographically
localized in taxa with lower dispersal (stronger IBD), larger local
population size (higher average heterozygosity) or more stable
population size assessed using departure from mutation-drift equilibrium
(i.e. lower absolute Tajima’s D). We apply this comparative approach to
the lizard fauna of the Australian Monsoonal Tropics (AMT).
The AMT is a diverse and biologically rich region characterized by
disjunct sandstone plateaus or areas of relatively high topographic
relief separated by regions of flat savanna woodland (Figure 1). Aridity
increases from north to south (Figure 1A). The AMT has strongly
contrasting rainfall across wet and dry seasons, set against
consistently warm temperatures (Figure 1B), and is the most fire-prone
region in Australia (Bowman et al., 2010). Previous studies identified
three biogeographically distinct areas within the AMT — the Top End,
Kimberley and Cape York Peninsula (Figure 1A; Bowman et al., 2010;
Woinarski, Mackey, Nix, & Traill, 2007), with the latter being the most
biogeographically distinct (Fujita, McGuire, Donnellan, & Moritz, 2010;
Lee & Edwards, 2008; Smith, Harmon, Shoo, & Melville, 2011). The Top
End is more mesic than the Kimberley (Figure. 1A). Large river plains
separate major plateaus in both regions (Figure 1A) and, along with
climatic and edaphic barriers (e.g. the Gulf plains and Ord arid
intrusion), represent a potential driver of allopatric divergence within
terrestrial species (Catullo, Lanfear, Doughty, & Keogh, 2014;
Eldridge, Potter, & Cooper, 2011).
Recent multilocus phylogeographic analyses of the AMT lizard fauna have
consistently revealed strong phylogeographic structure within
taxonomically recognized species. In some cases, cryptic species
complexes have subsequently been taxonomically revised (Afonso Silva et
al., 2017; Doughty et al., 2018; Melville, Date, Horner, & Doughty,
2019; Oliver et al., 2019; 2020), while assessments of species
boundaries for other groups are still in progress (Catullo et al., 2014;
Fujita et al., 2010; Laver, Doughty, & Oliver, 2018; Laver, Nielsen,
Rosauer, & Oliver, 2017; Melville, Ritchie, Chapple, Glor, & Li, 2011;
Potter et al., 2018). In some taxa (notably rock-specialist geckos;
Laver et al., 2018; Moritz et al., 2018; Oliver et al., 2020) this
phylogeographic structure can occur at very fine spatial scales, whereas
in other taxa (e.g. more generalist Carlia skinks, Afonso Silva
et al., 2017); Diporiphora dragons, Smith et al., 2011); andHeteronotia geckos, Moritz et al., 2016) the phylogeographic
units typically span broader geographic ranges (Figure 1C).
Phylogeographic lineages (whether or not now reclassified as separate
species) are also much older in Gehyra than are those in the
other genera (Figure 1C). There are also regional differences relating
to climate and topography. Short-range phylogeographic lineages are
concentrated in the more mesic regions of the Top End and west
Kimberley, including on islands (Rosauer et al., 2016, 2018) and
isolated karst limestones (Oliver et al., 2017). For Carlia, there were
more variable demographic responses to past climate change in the drier
Kimberley than the more mesic Top End (Potter et al., 2018).
This variation in the spatial and temporal scale of phylogeographic
structure provides the opportunity to apply landscape genetics within
lineages to test how intrinsic dispersal limits and ecological
specialization interact with environmental heterogeneity in shaping the
scale of phylogeographic structure within species. Using newly obtained
SNP data and landscape-scale sampling with phylogeographic lineages, we
1) tested whether dispersal limitation within lineages (IBD) varies
among taxa (families), ecologies (habitat requirement) or environmental
condition; 2) explored what environmental features best explain genetic
divergence within lineages (Isolation by
distance/resistance/environment); and 3) tested whether
microevolutionary processes, reflected in within-lineage genetic
parameters, explain differences among taxa in the geographic scale and
depth of phylogeographic lineages.
Material and Methods