DOI: 10.5061/dryad.zkh18937n
title: Data from: Does migration promote or inhibit diversification? A case study involving the dominant radiation of temperate Southern Hemisphere freshwater fishes

description: While theory predicts that dispersal is a pivotal influence on speciation
 and extinction rates, it can have contradictory effects on each, such that
 empirical studies are needed to quantify its role. In many studies,
 dispersal reduction appears to promote diversification, although some
 analyses of migratory species suggest otherwise. Here we test for a
 relationship between migratory status and diversification rate within the
 dominant radiation of temperate Southern Hemisphere freshwater fishes, the
 Galaxiidae. We reconstructed a molecular phylogeny for the group,
 comprising &gt;95% of extant lineages, and applied State-dependent
 Speciation Extinction models to estimate speciation, extinction, and
 diversification rates. In contrast to some previous studies, we revealed
 higher diversification rates in non-migratory lineages. The reduced gene
 flow experienced by non-migratory galaxiids appears to have increased
 diversification under conditions of allopatry or local adaptation.
 Migratory galaxiid lineages, by contrast, are genetically homogeneous
 within landmasses, but may also be rarely able to colonise other
 landmasses in the temperate Southern Hemisphere. The life history state
 exhibiting higher diversification likely reflects the spatial context of
 the study system relative to species dispersal abilities, by means of the
 intermediate dispersal model; the accurate quantification of dispersal
 abilities will aid in our understanding of these likely interactions.
description: Phylogenetic analyses incorporated as many galaxiid species as
 possible. While studies of diversification rates can accommodate missing
 taxa by incorporating their proportion during analysis, they assume the
 missing taxa are randomly distributed across the tree (Beaulieu and
 O’Meara 2016). However, the previously most comprehensive phylogenetic
 analysis of Galaxiidae (Burridge et al. 2012) lacks representation within
 two groups of morphologically cryptic species. Therefore, these groups
 were incorporated into the existing DNA dataset (599 bp
 <i>lrRNA</i>, 1154 bp cyt <i>b</i>, 1695 bp
 <i>RAG-1</i>, 1083 bp <i>S7</i>), and re-analysed
 to construct a time-calibrated phylogeny, following the same approach as
 previously (Burridge et al. 2012). Firstly, the South African
 <i>Galaxias zebratus</i> clearly represents a group of
 morphologically cryptic species (Waters and Cambray 1997; Chakona et al.
 2013). Cytochrome <i>b</i> data were added to represent the
 ‘nebula’, ‘Heuningnes’, ‘Klein’, ‘Joubertina’, ‘Riviersonderend’,
 ‘Goukou’, ‘Breede’, ‘rectognathus’, ‘slender’ and ‘mollis’ putative
 species (Waters and Cambray 1997; Chakona et al. 2013). Another distinct
 lineage previously identified from the Olifants River is also retained
 (Waters and Cambray 1997). Secondly, the Australian mountain galaxias
 complex (<i>Galaxias olidus s.l.</i>) is now recognised as a
 radiation comprising at least 15 species (Adams et al. 2014; Raadik 2014).
 While not all species within the mountain galaxias complex are
 reciprocally monophyletic for DNA variation (Raadik 2014), we chose cyt
 <i>b</i> sequences that represent a lineage distinct for each
 species. While the molecular phylogeny reconstructed for these
 recently-diverged mountain galaxias may not represent those of the actual
 species, all species exhibit the same life history and the chronology of
 their molecular divergence is very shallow. Following Adams et al. (2014)
 and Raadik (2014), the previously analysed data ascribed to <i>G.
 olidus</i> now corresponds to <i>G. oliros</i>. In
 addition to data from these two recently resolved complexes, cyt
 <i>b</i>, <i>lrRNA</i> and <i>S7</i>
 data from a new species <i>Galaxiella toourtkoourt</i>
 (Coleman et al. 2015) were also included. It has become apparent that
 previously analysed sequence data considered to represent
 <i>Aplochiton taeniatus</i> actually represents <i>A.
 zebra</i>, and therefore new cyt <i>b</i> data have been
 substituted. Homologous data from the recently resurrected <i>A.
 marinus</i> were not available at the time of analysis, representing
 the only excluded galaxiid species. All new data analysed relative to
 Burridge et al. (2012) are summarised in Table S1. The proportion of
 missing species was set at 0.07 for diadromous species (1/14), and 0.03
 (2/68) for non-diadromous species (estimating that two species may still
 not be recognised within <i>G. zebratus</i>
 <i>s.l.</i>, <i>G. olidus s.l.</i>, or
 elsewhere). The molecular phylogeny of the Galaxiidae,
 with branches scaled proportionally to evolutionary time, was obtained
 following the approach of Burridge et al. (2012). The analysis used a
 relaxed molecular clock and included nine biogeographic calibration points
 within the family, together with nine fossil age calibration points from
 outgroup lineages. BEAST 2.6.2 (Bouckaert et al. 2019) post-burnin run
 exceeded 6.9x10<sup>8</sup> steps, with stationarity and
 convergence assessed using Tracer (Rambaut et al. 2018). 35,586 trees were
 retained for the construction of a maximum clade credibility tree using
 TreeAnnotater. This tree was well resolved at most nodes, with topological
 uncertainty generally restricted to shallow nodes that do not involve
 transitions in diadromy status. Outgroups and lineages that represent
 intraspecific galaxiid divergences were pruned such that each galaxiid
 species was represented by a single lineage, with two exceptions. First,
 the diadromous <i>Galaxias brevipinnis</i> is resolved as
 polyphyletic, with New Zealand and Australian clades exhibiting molecular
 divergence consistent with interspecific differentiation elsewhere in the
 family (Waters et al. 2010; Burridge et al. 2012). Secondly,
 <i>Galaxias maculatus</i> exhibits substantial molecular
 divergence among Australian, New Zealand, and South American populations,
 and arguably represents three species (Waters and Burridge 1999).
 <i>Galaxias niger</i> was excluded as this appears to be
 synonymous with Australian <i>G. brevipinnis</i> based on the
 depth of molecular divergence and morphological plasticity of the
 latter. Taxa were coded as diadromous or non-diadromous
 based on knowledge derived from published accounts of species biology
 (largely summarised by Augspurger et al. 2017). Observations of migratory
 status of <i>Aplochiton</i> spp. indicate that populations of
 <i>A. taeniatus</i> might variously be freshwater-resident or
 diadromous (catadromous or amphidromous), and some landlocked populations
 are known also for <i>A. zebra</i> (Alò et al. 2019). The
 widespread distribution of the latter (including the Falkland Islands /
 Islas Malvinas), however, implies a recent diadromous history, and
 therefore this species was considered to possess both life histories.
 Semi-anadromy is observed in <i>Lovettia</i> (Schmidt et al.
 2014), the sister-lineage of <i>Aplochiton</i>. The majority
 of diadromous species also exhibit landlocked populations
 (<i>Aplochiton</i> spp., <i>G.
 brevipinnis</i>-Australia and New Zealand, <i>Galaxias
 maculatus</i>, <i>Galaxias truttaceus</i>,
 <i>Galaxias argenteus</i>, <i>Galaxias
 fasciatus</i>), and were treated in two ways. Firstly, they were
 coded as diadromous, because their landlocked populations are likely
 recent derivatives of diadromous populations, which better reflects their
 state through evolutionary time (Ovenden et al. 1993; Waters et al. 2010).
 Secondly, we also tested models under which species could occupy multiple
 states simultaneously (using GeoHiSSE, below). Analyses
 were conducted under the Hidden-state Speciation Extinction (HiSSE)
 framework (Beaulieu and O’Meara 2016) to test the null hypothesis of no
 relationship between diversification rate and migratory status. This
 approach avoids potential errors associated with the use of “equal rate”
 null hypotheses (Rabosky and Goldberg 2015), and also accommodates shifts
 in diversification that could also be related to states that are
 unobserved or “hidden”, to reduce inferential errors with respect to
 migratory status (Beaulieu and O’Meara 2016). All analyses were performed
 in R using the <i>hisse</i> (Beaulieu and O’Meara 2016) and
 <i>diversitree</i> (FitzJohn 2012) packages. The parameters of
 the HiSSE model are rates of transition among character states (diadromy,
 hidden state: presence/absence), and species turnover (speciation +
 extinction) and extinction fraction (extinction/speciation). State
 transition rates (diadromous&lt;-&gt;non-diadromous) were either
 equal or unequal. Simultaneous changes in migration status and the hidden
 state were excluded. The null model assumed that species turnover and
 extinction fraction did not vary with respect to migratory status, but did
 with respect to hidden state (“A” or “B”). The null was then compared to a
 model lacking hidden states, where species turnover and extinction
 fraction were allowed to vary with migratory status. Models were compared
 based on Akaike information criterion (AIC). Additional models were
 constructed to test whether the presence of hidden states within either
 diadromous or non-diadromous lineages could explain an apparent difference
 in diversification with respect to migratory status (Beaulieu and O’Meara
 2016). A contribution of a nested hidden state to diversification might
 reveal that additional characteristics are also important in explaining
 diversification rates (Beaulieu and O’Meara 2016).
 Models were also conducted under the GeoHiSSE framework (Caetano
 et al. 2018), originally developed for biogeographic analysis where
 species can occupy multiple areas, but here applied to accommodate those
 species exhibiting both diadromous and non-diadromous populations (see
 list above). Analyses analogous to HiSSE were performed using the
 <i>hisse</i> package. These analyses allowed transitions
 directly between diadromy and non-diadromy (no requirement of a
 polymorphic intermediate state; “include.jumps=TRUE”) and also from a
 dispersal-polymorphic state to either of these individual states
 (“separate.extirpation=TRUE”).