Benjamin Douglas Cook

Biogeographic history of an Australian freshwater shrimp, Paratya australiensis (Atyidae): the role life history transition in phylogeographic diversification

The widespread distribution of the freshwater shrimp Paratya australiensis in eastern Australia suggests that populations of this species have been connected in the past. Amphidromy is ancestral in these shrimps, although many extant populations are known to be restricted to freshwater habitats. In this study, we used a fragment of the cytochrome c oxidase I mitochondrial DNA (mtDNA) gene to examine diversity within P. australiensis and to assess the relative importance of amphidromy in its evolutionary history. We hypothesized that if transitions from an amphidromous to a freshwater life history were important, then we would find a number of divergent lineages restricted to single or groups of nearby drainages. Alternatively, if amphidromy was maintained within the species historically, we expected to find lineages distributed over many drainages. We assumed that the only way for divergence to occur within amphidromous lineages was if dispersal was limited to between nearby estuaries, which, during arid periods in the earths history, became isolated from one another. We found nine highly divergent mtDNA lineages, estimated to have diverged from one another in the late Miocene/early Pliocene, when the climate was more arid than at present. Despite this, the geographic distribution of lineages and haplotypes within lineages did not support the notion of a stepping‐stone model of dispersal between estuaries. We conclude that the extensive divergence has most likely arisen through a number of independent amphidromy–freshwater life history transitions, rather than via historical isolation of amphidromy populations. We also found evidence for extensive movement between coastal and inland drainages, supporting the notion that secondary contact between lineages may have occurred as a result of drainage rearrangements. Finally, our data indicate that P. australiensis is likely a complex of cryptic species, some of which are widely distributed, and others geographically restricted.

Marine dispersal determines the genetic population structure of migratory stream fauna of Puerto Rico: evidence for island-scale population recovery processes

Abstract Various components of island stream faunas, including caridean shrimps, fish, and gastropods, undertake obligate amphidromous migration, whereby larvae are released in upstream freshwater reaches, drift downstream to estuaries or marine waters, then migrate upstream as postlarvae to freshwater adult habitats. Longitudinal migration from estuaries to headwaters is well documented for many amphidromous species, but the degree of among-river marine dispersal is poorly known for most species. We need better understanding of the potential for marine dispersal in population processes of amphidromous species, particularly recolonization and population recovery in impacted lotic systems, such as those on Puerto Rico, because some theories of dispersal for species with marine larvae predict high rates of self-recruitment. We tested population genetic predictions for widespread marine larval dispersal and self-recruitment to the natal river for 11 amphidromous species, including shrimps, fish, and a gastropod, in Puerto Rico. Population genetic analysis of mitochondrial DNA data showed high rates of gene flow among rivers and indicated that marine dispersal determines the population genetic structure of all 11 species. Difficulty in recruiting to oceanic currents promotes closed population structures in some marine species, but larvae of amphidromous species entrained in downstream river flow might be delivered more readily to ocean currents. Population recovery processes occurred at the island scale rather than at the river scale, but further studies are needed to identify whether population recovery processes are likely at larger spatial scales (e.g., among islands). River management strategies should maintain environmental flows that allow larval export, maintain longitudinal dispersal pathways over dam spillways and via subterranean passages, and maintain open and healthy estuaries.

Molecular evidence for sequential colonization and taxon cycling in freshwater decapod shrimps on a Caribbean island

Taxon cycling, i.e. sequential phases of expansions and contractions in species’ distributions associated with ecological or morphological shifts, are postulated to characterize dynamic biogeographic histories in various island faunas. The Caribbean freshwater shrimp assemblage is mostly widespread and sympatric throughout the region, although one species (Atyidae: Atya lanipes) is geographically restricted and ecologically and morphologically differentiated from other Atya species. Using patterns of nucleotide variation at the COI mtDNA gene in five species of freshwater shrimp (A. lanipes, A. scabra, A. innocuous; Xiphocarididae: Xiphocaris elongata; Palaemonidae: Macrobrachium faustinum) from Puerto Rico, we expected to detect a signature of sequential colonization in these shrimp, consistent with the concept of taxon cycling, and expected that A. lanipes would be at a different taxon stage (i.e. an early stage species) to all other species. We also examined patterns of genetic population structure in each species expected with poor, intermediate and well‐developed abilities for among‐river dispersal. Population expansions were detected in all species, although the relative timing of the expansions varied among them. Assuming that population expansions followed colonization of Puerto Rico by freshwater shrimp, results bear the hallmarks of sequential colonization and taxon cycling in this fauna. A. lanipes had a star phylogeny, low mean pairwise nucleotide differences and recent (Holocene) estimates for an in situ population expansion in Puerto Rico, and it was inferred as an early stage species in the taxon cycle undergoing a secondary phase of expansion. All other species were inferred as late stage species undergoing regional population expansions, as their mean pairwise nucleotide differences were relatively high and phylogenetic patterns were more complex than A. lanipes. High rates of gene flow without isolation by distance among rivers were detected in all species, although results should be treated cautiously as some populations are unlikely to be in mutation–drift equilibrium. Nested clade analysis produced inconsistent results among species that all have high rates of gene flow and expanding populations.

Phylogeography of an Island Endemic, the Puerto Rican Freshwater Crab (Epilobocera sinuatifrons)

The endemic Puerto Rican crab, Epilobocera sinuatifrons (Pseudothelphusidae), has a freshwater-dependant life-history strategy, although the species has some capabilities for terrestrial movement as adults. In contrast to all other freshwater decapods on the island (e.g., caridean shrimp), E. sinuatifrons does not undertake amphidromous migration, and is restricted to purely freshwater habitats and adjacent riparian zones. As Puerto Rico has a dynamic geologic history, we predicted that both the life history of E. sinuatifrons and the geological history of the island would be important determinants of phylogeographic structuring in the species. Using a fragment of the cytochrome c oxidase subunit 1 mtDNA (mitochondrial DNA) gene, we tested for deviations from panmixia among and within rivers draining Puerto Rico and used statistical phylogeography to explore processes that may explain extant patterns of genetic variation in the species. While populations of E. sinuatifrons were significantly differentiated among rivers, they were likely to be recently derived because nested clade analysis (NCA) indicated evolutionarily recent restricted gene flow with isolation by distance (IBD) and contiguous range expansion at various spatial scales. Ongoing drainage rearrangements associated with faulting and land slippage were invoked as processes involved in sporadic gene flow among rivers throughout the Pleistocene. Patterns of genetic differentiation conformed to IBD and population demographic statistics were nonsignificant, indicating that although recently derived, populations from different rivers were in drift-mutation equilibrium. A shallow (0.6 million years ago), paraphyletic split was observed in the haplotype network, which NCA indicated arose via allopatric fragmentation. This split coincides with an area of high relief in central Puerto Rico that may have experienced relatively little drainage rearrangements. Shallow but significant genetic isolation of populations of E. sinuatifrons among Puerto Rican rivers suggests phylogeographic patterns that are intermediate to terrestrial habitat specialists (highly divergent populations) and other freshwater biota, such as amphidromous species and insects with aerial adult dispersal (highly connected populations).

Evolutionary relationships of atyid shrimps imply both ancient Caribbean radiations and common marine dispersals

Abstract The evolutionary relationships of the surface genera of shrimps of the family Atyidae from the Caribbean were inferred using mitochondrial 16S ribosomal DNA and cytochrome oxidase I gene sequences. The genetic divergence among the 4 Caribbean genera (Atya, Jonga, Micratya, Potimirim) is extensive and dates from between the Eocene and Miocene. This result suggests a vicariant origin or the ancient dispersal of some taxa. Most intrageneric divergences date to the late Miocene–Pliocene and, thus, are probably the result of dispersal. Some species show low levels of intraspecific genetic divergence between distant islands, and thus, present-day or geologically recent gene flow is likely. This gene flow is probably a consequence of the amphidromous life histories of most Caribbean freshwater shrimps. Despite the ancient divergences between the genera, the Caribbean surface atyids form a single evolutionary lineage when compared with atyid shrimp from throughout the world, and this result implies an ancient evolutionary radiation in the Caribbean. The sister group to the Caribbean atyids are the large-bodied and robust Atya-like shrimps of the Indo-Pacific, which share a similar size and shape with Caribbean Atya. Thus, the common ancestor probably was also large and robust. In contrast, the other Caribbean atyids are much smaller, and Jonga has a distinct morphology that is associated with a switch from lotic to lentic environments. This radiation may have been the result of the absence from the Caribbean of other small shrimps that are common in the Indo-Pacific.

Broadscale phylogeographic structure of five freshwater fishes across the Australian Monsoonal Tropics

Abstract: The Australian Monsoonal Tropics (AMT) is a unique location for the study of phylogeography and intraspecific genetic variation in freshwater fish. We assessed the phylogeographic structure of 5 species from 2 genera across the region. The species included 3 neosilurids (Plotosidae, Neosilurus hyrtlii, Neosilurus ater, and Neosilurus pseudospinosus) and 2 members of the genus Oxyeleotris (Eleotridae, O. selheimi and O. lineolata). We used mitochondrial deoxyribonucleic acid (mtDNA) and phylogenetic analyses to explore the phylogeographic histories of these species. Overall, phylogeographic patterns were inconsistent. Some species were highly structured, and phylogeographic breaks were detected (e.g., N. hyrtlii, N. pseudospinosus, and O. selheimi), but other species showed no obvious divergences across the AMT (N. ater and O. lineolata). All species sampled in the Gulf of Carpentaria had shallow phylogenies, consistent with the expectation that historically, Lake Carpentaria would have provided connectivity through this region. All species also showed evidence of recent connectivity across drainage divides on the eastern and western coasts of the Cape York Peninsula. Some species in the Kimberley region were highly structured, consistent with expectation that these ancient and geologically stable catchments would promote divergence in allopatry. Conservation efforts should now be directed toward ensuring that the intraspecific biodiversity identified in our study and others are protected in the future.

Historical population connectivity and fragmentation in a tropical freshwater fish with a disjunct distribution (pennyfish, Denariusa bandata)

Abstract Pennyfish, Denariusa bandata, are small freshwater fish widely distributed in northern Australia in 4 highly disjunct regions and in the Fly River and Bensbach River drainages in southern Papua New Guinea (PNG). Alternating phases of exposure of the Australia–New Guinea Continental Shelf (ANGCS) during stands of lowered sea levels during Pleistocene glacial phases created a land bridge and fresh/brackish water habitats that intermittently connected Australia and PNG. Some biogeographic theories and empirical evidence for several freshwater crustaceans suggest that wetlands on the exposed ANGCS during the last glacial maximum were an important conduit for dispersal and gene flow in freshwater species between Australia and PNG and across northern Australia and that connectivity was severed by the most recent sea level rise in the region (∼6–8 thousand years before present). We used mitochondrial deoxyribonucleic acid (mtDNA) sequence data to test phylogeographic hypotheses concerning the origin of the disjunct distribution in D. bandata in relation to dispersal–vicariant processes and exposure of the ANGCS during Pleistocene sea level changes. Rather than a late Pleistocene origin associated with the last glacial maximum, the coalescence of the regional populations was in the early- to mid-Pleistocene, and the molecular data indicated that the eastern regional populations split before the northern populations split (i.e., sequential vicariance), whereas the northern populations split contemporaneously (i.e., simultaneous vicariance). The complex mtDNA genealogy for D. bandata also indicated a phylogeographic history in which ancestral lineages were retained in the northwestern part of its distribution, and ancestral haplotype diversity was retained in the Fly River (PNG) population because several divergent clusters of PNG haplotypes were more closely related to Australian haplotypes than to each other.

Species diversity and genetic differentiation of stygofauna (Syncarida : Bathynellacea) across an alluvial aquifer in north-eastern Australia

Abstract. Recent research suggests that alluvial aquifers in southern and eastern Australia may contain a diverse subterranean aquatic fauna (i.e. stygofauna). However, to date only a limited number of alluvial aquifers have been studied and little molecular data are available to assess species-level diversity and spatial patterns of genetic variation within stygofaunal species. In this paper, we present the initial results of a stygofaunal survey of the Burdekin River alluvial aquifer in Queensland, extending the northern range of alluvial aquifers along the east coast of Australia that have been investigated. The survey resulted in the collection of bathynellid stygofauna (Syncarida: Bathynellacea) and genetic analyses were conducted to determine species level diversity using the mitochondrial cytochrome oxidase subunit I (COI) gene. We further investigated the phylogenetic relationships of the species with bathynellids from western and southern Australia to assess the generic status of species. Four highly divergent COI lineages within the Parabathynellidae and one lineage within the Bathynellidae were found. These lineages did not group within any described genera, and phylogenetic analyses indicated that both local radiations and the retention of a lineage that was more apical in the genealogy account for the diversity within the Parabathynellidae in the Burdekin River alluvial aquifer. Most COI lineages were sampled from only a single bore, although one taxon within the Parabathynellidae was found to be more widespread in the aquifer. Haplotypes within this taxon were not shared among bores (ΦST = 0.603, P < 0.001). Overall, the high species diversity for bathynellaceans from an alluvial aquifer reported here, and surveys of bathynellaceans in several other alluvial systems in south-eastern Australia, suggests that groundwater ecosystems of eastern Australia may contain high stygofaunal diversity by Australian and world standards, particularly at the generic level for parabathynellids.

Did common disjunct populations of freshwater fishes in northern Australia form from the same biogeographic events

Abstract: Several freshwater fishes have disjunct (geographically discrete and widely spaced) distributions across northern Australia. We used mitochondrial deoxyribonucleic acid (mtDNA) data and phylogeographic analyses to examine the origin of these common disjunct distributions and to test the hypothesis that they were a result of a single biogeographic event. These disjunct distributions are not perfectly shared among species, but we selected 3 species that have wide ranges with the most similar disjunct geographic overlap: Spotted Blue Eye (Pseudomugil gertrudae), Pennyfish (Denariusa australis), and MacCullochs Rainbow Fish (Melanotaenia maccullochi). Despite similarity in their present-day disjunct distributions, spatial genetic patterns varied considerably among the 3 species in terms of measures of molecular diversity, number of mtDNA lineages within each species, inter- and intra-regional spatial distribution of individual lineages within species, and degree of partitioning of genetic variation among regions. Pseudomugil gertrudae and D. australis each contained 1 to 2 divergent lineages at particular sites in 1 of the regions (Top End), but both species also contained lineages in this region that were more closely related to conspecific populations in other regions. Two regional populations (Top End and Northern Cape York Peninsula) of M. maccullochi consisted exclusively of highly divergent lineages that probably reflect cryptic species. When the divergent lineages within each species were excluded from temporal analyses, a single vicariant event among regions could not be rejected. Our results indicate that several regional populations are long-term relicts for M. maccullochi and that several sites within Top End are associated with localized long-term refugia for P. gertrudae and D. australis. A single biogeographic event in the mid- to late-Pleistocene may have created broadscale separation of most populations of these species.

Accurate systematic frameworks are vital to advance ecological and evolutionary studies, with an example from Australian freshwater fish (Hypseleotris)

The practice of modern evolutionary and ecological research is interdisciplinary, with the process of evolution underpinning the diversity on display. However, the inference of evolutionary patterns can be difficult owing to their historical nature. When the biological units and evolutionary relationships involved are unclear, interpreting any ecological and biological data can be problematic. Herein we explore resulting issues when evolutionary theories rely on an unclear or incomplete biological framework, using some Australian freshwater fish (carp gudgeons: Hypseleotris, Eleotridae) as an example. Specifically, recent theories regarding the role of developmental plasticity on ontogeny and speciation have focused on this group. However, carp gudgeons have complex, and as yet incompletely understood, species boundaries and reproductive biology. Even basic data for the recognised taxa, relating to their phylogenetic relationships, life histories and species distributions, are unclear, have often been misinterpreted and are still in the process of being assembled. Combined, these factors make carp gudgeons a relatively poor group on which to apply more advanced evolutionary theories at the moment, such as the role of developmental plasticity in diversification.