Matthew J. Larcombe

Transient hybridization, not homoploid hybrid speciation, between ancient and deeply divergent conifers

PREMISE OF THE STUDY Homoploid hybrid speciation is receiving growing attention due the increasing recognition of its role in speciation. We investigate if individuals intermediate in morphology between the two species of the conifer genus Athrotaxis represent a homoploid hybrid species, A. laxifolia, or are spontaneous F1 hybrids. METHODS A total of 1055 individuals of Athrotaxis cupressoides and A. selaginoides, morphologically intermediate individuals, and two putative hybrid swarms were sampled across the range of the genus and genotyped with 13 microsatellites. We used simulations to test the power of our data to identify the pure species, F1s, F2s, and backcross generations. KEY RESULTS We found that Athrotaxis cupressoides and A. selaginoides are likely the most divergent congeneric conifers known, but the intermediates are F1 hybrids, sharing one allele each from A. cupressoides and A. selaginoides at six loci with completely species specific alleles. The hybrid swarms contain wide genetic variation with stronger affinities to the locally dominant species, A. selaginoides and A. selaginoides backcrosses outnumbering A. cupressoides backcrosses. In addition, we observed evidence for isolated advanced generation backcrosses within the range of the pure species. CONCLUSIONS We conclude that, even though they can be large and long-lived, Athrotaxis hybrid swarms are on a trajectory of decline and will eventually be reabsorbed by the parental species. However, this process may take millennia and fossil evidence suggests that such events have occurred repeatedly since the early Quaternary. Given this timeline, our study highlights the many obstacles to homoploid hybrid speciation.

Dormancy in Caladenia: a Bayesian approach to evaluating latency

Dormancy is common in many terrestrial orchids in southern Australia and other temperate environments. The difficulty for conservation and management when considering dormancy is ascertaining whether non-emergent plants aredormantordead.Hereweuseamulti-statecapture-recapturemethod,undertakenoverseveralseasons,todeterminethe likelihood of a plant becoming dormant or dying following its annual emergent period and evaluate the frequency of the lengthofdormancy.Weassessthetransitionprobabilitiesfromtimeseriesofvaryinglengthsforthefollowingnineterrestrial orchids in the genus Caladenia: C. amoena, C. argocalla, C. clavigera, C. elegans, C. graniticola, C. macroclavia, C. oenochila,C. rosella and C. valida from Victoria, South Australia and Western Australia. We used a Bayesian approach for estimating survivorship, dormancy and the likelihood of death from capture-recapture data. Considering all species together, the probability of surviving from one year to the next was ~86%, whereas the likelihood of observing an individual above ground in two consecutive years was ~74%. All species showed dormancy of predominantly 1 year, whereasdormancyofthreeormoreyearswasextremelyrare(<2%).Theresultshavepracticalimplicationsforconservation, in that (1) population sizes of Caladenia species are more easily estimated by being able to distinguish the likelihood of an unseen individual being dormant or dead, (2) population dynamics of individuals can be evaluated by using a 1-3-year dormancy period and (3) survey effort is not wasted on monitoring individuals that have not emerged for many years.

Managing Australia’s eucalypt gene pools: assessing the risk of exotic gene flow

Most eucalypts are endemic to Australia but they have been introduced into more than 100 countries and there are now over 20 million hectares of eucalypt plantations globally. These plantations are grown mainly for pulpwood but there is expanding interest in their use as a renewable source of solid wood products and energy. In Australia, the eucalypt plantation estate is nearing one million hectares, located mainly in temperate regions and dominated by Eucalyptus globulus and E. nitens (subgenus Symphyomyrtus), which are grown mainly outside their natural ranges. While eucalypt species from different major subgenera do not hybridise, hybrids within subgenera are often reported, including hybrids with plantation species. Concerns were raised in the late 1990s that pollen-mediated gene flow from locally exotic plantation eucalypts may affect the integrity of adjacent native eucalypt gene pools. As Australia is the centre-of-origin of most eucalypt species used in plantations around the world, exotic gene flow is one of the many issues that require management for industry sustainability and certification purposes. We here summarise over a decade of research aimed at providing the framework and biological data to help assess and manage the risk of gene flow from these plantations into native gene pools in Australia.

Assessing a Bayesian Approach for Detecting Exotic Hybrids between Plantation and Native Eucalypts

Eucalyptus globulus is grown extensively in plantations outside its native range in Australia. Concerns have been raised that the species may pose a genetic risk to native eucalypt species through hybridisation and introgression. Methods for identifying hybrids are needed to enable assessment and management of this genetic risk. This paper assesses the efficiency of a Bayesian approach for identifying hybrids between the plantation species E. globulus and E. nitens and four at-risk native eucalypts. Range-wide DNA samples of E. camaldulensis, E. cypellocarpa, E. globulus, E. nitens, E. ovata and E. viminalis, and pedigreed and putative hybrids (n = 606), were genotyped with 10 microsatellite loci. Using a two-way simulation analysis (two species in the model at a time), the accuracy of identification was 98% for first and 93% for second generation hybrids. However, the accuracy of identifying simulated backcross hybrids was lower (74%). A six-way analysis (all species in the model together) showed that as the number of species increases the accuracy of hybrid identification decreases. Despite some difficulties identifying backcrosses, the two-way Bayesian modelling approach was highly effective at identifying , which, in the context of E. globulus plantations, are the primary management concern.

Population dynamics of Caladenia: Bayesian estimates of transition and extinction probabilities

A disproportionate number of threatened plant species in Australia are found in the genus Caladenia, although little has been published on their life history. Here we examine data from nine species to evaluate some of the basic life-history strategies in Caladenia, specifically the transitions between life-history stages. We constructed life-history transition models of the orchids by using a Bayesian approach, we evaluated the growth rate of populations, compared transition values among species and determined which stage influenced the population growth most. We assessed extinction likelihood and considered the effect of variation in transitions among states on the probability of extinction. Bayesian model selection showed differences between species regarding their life cycle. The probability of individuals flowering in two consecutive years is extremely rare and was found to be common in only one species, C. amoena. All other species had a high likelihood of returning to a vegetative state, and some were likely to enter dormancy after flowering. High elasticities in the transition from the dormant to dormant stage suggest that dormancy has a large impact on population persistence. The quasi-extinction rate suggests that C. rosella, C. clavigera, C. graniticola and C. macroclavia are most at risk when all species have an equal initial population size. Conservation management should focus on studies to identify cues that influence flowering in consecutive years, emergence from dormancy and increasing recruitment.

Understanding the naturalization of Eucalyptus globulus in Portugal: a comparison with Australian plantations

Despite the potential utility of a biogeographical approach to understanding the naturalization of exotic species, studies using this approach are scarce. Eucalyptus globulus is an economically important Australian tree species that has become naturalized in a number of countries where it was introduced. Portugal is an ideal territory to study the naturalization of E. globulus owing to: a long introduction history, the antipodal location compared to Australia and the large cultivated area. Wildling density was assessed in 116 E. globulus plantations in central Portugal through 213 transects established along plantation borders. Boosted regression trees were used to model the influence of plantation-scale variables. Results from this survey were compared with data obtained in plantations from seven Australian regions, where a similar sampling protocol had been used. In Portugal, wildlings were more abundant in plantations that were: located in moist aspects, coppiced, with older tree stems and corresponding to intermediate site growth indexes. The overall density (127 plants ha−1) was 14.9 times higher than in the Australian estate, but this ratio was reduced to 3.1 in a more comparable subset of unburnt, first rotation plantations. A generalized linear model fitted using a dataset combining the two surveys showed that country influenced wildling density, together with plantation rotation and stem age. These results provide insights into the naturalization of a widely cultivated tree species, pointing to a fundamental role of the introduction history, possibly acting along with the biogeographical characteristics of the introduced range.

On the persistence of reproductive barriers in Eucalyptus: the bridging of mechanical barriers to zygote formation by F1 hybrids is counteracted by intrinsic post-zygotic incompatibilities

BACKGROUND AND AIMS Many previous studies conclude that pre-zygotic barriers such as mechanical isolation account for most reproductive isolation between pairs of taxa. However, the inheritance and persistence of barriers such as these after the first generation of hybridization is rarely quantified, even though it is a vital consideration in understanding gene flow potential. There is an asymmetrical pre-zygotic mechanical barrier to hybridization between Eucalyptus nitens and Eucalyptus globulus, which completely prevents small-flowered E. nitens pollen from mating with large E. globulus flowers, while the reverse cross is possible. We aimed to determine the relative importance of pre- and post-zygotic barriers in preventing gene flow following secondary contact between E. nitens and E. globulus, including the inheritance of barriers in advanced-generation hybrids. METHODS Experimental crossing was used to produce outcrossed E. nitens, E. globulus and their F1, F2, BCg and BCn hybrids. The strength and inheritance of a suite of pre- and post-zygotic barriers were assessed, including 20-year survival, growth and reproductive capacity. KEY RESULTS The mechanical barrier to hybridization was lost or greatly reduced in the F1 hybrid. In contrast, intrinsic post-zygotic barriers were strong and persistent. Line-cross analysis indicated that the outbreeding depression in the hybrids was best explained by epistatic loss. CONCLUSIONS The removal of strong mechanical barriers between E. nitens and E. globulus allows F1 hybrids to act as a bridge for bi-directional gene flow between these species. However, strong and persistent post-zygotic barriers exist, meaning that wherever F1 hybridization does occur, intrinsic post-zygotic barriers will be responsible for most reproductive isolation in this system. This potential transient nature of mechanical barriers to zygote formation due to additive inheritance in hybrids appears under-appreciated, and highlights the often important role that intrinsic post-mating barriers play in maintaining species boundaries at zones of secondary contact.

Greater range filling can explain why evolutionarily older and slower diversifying plants are less threatened by extinction

Extinction threatens many species, yet few factors predict this risk across the plant Tree of Life (ToL). Taxon age is one factor that may associate with extinction if occupancy of geographic and adaptive zones varies with time. Age-dependent occupancy can also influence diversification rates and thus extinction risk where new taxa have small range and population sizes. Here we found that faster diversifying plant genera had more species threatened by extinction across the ToL. Evolutionary age had no effect in 297 sampled genera, potentially because they were older, on average, than expected. Repeating our analyses in two large, well-sampled groups, we found that extinction risk decreased with evolutionary age in conifer species but not palms. Range filling increased in older, non-threatened conifers more strongly than in threatened taxa. Our results suggest contrasting modes of speciation may explain differing patterns of extinction risk across the ToL with consequences for biodiversity conservation.Many species are threatened by extinction, yet few factors have been identified to explain this risk across the plant Tree of Life (ToL). Lineages that are evolutionarily younger or occurring within rapidly diversifying clades may have elevated extinction risk because they occupy smaller geographic ranges and adaptive zones as compared with older lineages that have tolerated longer periods of environmental change. Here we find that faster diversifying plant genera had more species at risk of extinction. Evolutionary age had no effect in the 297 genera that we sampled, potentially because of sampling older genera, on average, from across the ToL. Repeating our analyses in two well-sampled and large groups, we found that extinction risk decreased with evolutionary age in conifer species but not palms. Small sample sizes limited our power to detect effects of lineage diversification in these groups. Our results suggest that contrasting modes of speciation may explain differing patterns of extinction risk across the broader ToL and have consequences for biodiversity conservation.

Range size dynamics can explain why evolutionarily age and diversification rate correlate with contemporary extinction risk in plants

Extinction threatens many species, yet few factors predict this risk across the plant Tree of Life (ToL). Taxon age is one factor that may associate with extinction if occupancy of geographic and adaptive zones varies with time. Age-dependent occupancy can also influence diversification rates and thus extinction risk where new taxa have small range and population sizes. Here we found that faster diversifying plant genera had more species threatened by extinction across the ToL. Evolutionary age had no effect in 297 sampled genera, potentially because they were older, on average, than expected. Repeating our analyses in two large, well-sampled groups, we found that extinction risk decreased with evolutionary age in conifer species but not palms. Range filling increased in older, non-threatened conifers more strongly than in threatened taxa. Our results suggest contrasting modes of speciation may explain differing patterns of extinction risk across the ToL with consequences for biodiversity conservation.Many species are threatened by extinction, yet few factors have been identified to explain this risk across the plant Tree of Life (ToL). Lineages that are evolutionarily younger or occurring within rapidly diversifying clades may have elevated extinction risk because they occupy smaller geographic ranges and adaptive zones as compared with older lineages that have tolerated longer periods of environmental change. Here we find that faster diversifying plant genera had more species at risk of extinction. Evolutionary age had no effect in the 297 genera that we sampled, potentially because of sampling older genera, on average, from across the ToL. Repeating our analyses in two well-sampled and large groups, we found that extinction risk decreased with evolutionary age in conifer species but not palms. Small sample sizes limited our power to detect effects of lineage diversification in these groups. Our results suggest that contrasting modes of speciation may explain differing patterns of extinction risk across the broader ToL and have consequences for biodiversity conservation.

The dimensions of species diversity

Diversification processes underpin the patterns of species diversity that fascinate biologists. Two competing hypotheses disagree about the effect of competition on these processes. The bounded hypothesis suggests that species diversity is limited (bounded) by competition between species for finite niche space, while the unbounded hypothesis proposes that evolution and ecological opportunity associated with speciation, render competition unimportant. We use phylogenetically structured niche modelling, to show that processes consistent with both these diversification models have driven species accumulation in conifers. In agreement with the bounded hypothesis, niche competition constrained diversification, and in line with the unbounded hypothesis, niche evolution and partitioning promoted diversification. We then analyse niche traits to show that these diversification enhancing and inhibiting processes can occur simultaneously on different niche dimensions. Together these results suggests a new hypothesis for lineage diversification based on the multi-dimensional nature of ecological niches that accommodates both bounded and unbounded diversification processes.