Multiple Continental Radiations and Correlates of Diversification in Lupinus (Leguminosae): Testing for Key Innovation with Incomplete Taxon Sampling

Abstract

Replicate radiations provide powerful comparative systems to address questions about the interplay between opportunity and innovation in driving episodes of diversification and the factors limiting their subsequent progression. However, such systems have been rarely documented at intercontinental scales. Here, we evaluate the hypothesis of multiple radiations in the genus Lupinus (Leguminosae), which exhibits some of the highest known rates of net diversification in plants. Given that incomplete taxon sampling, background extinction, and lineage-specific variation in diversification rates can confound macroevolutionary inferences regarding the timing and mechanisms of cladogenesis, we used Bayesian relaxed clock phylogenetic analyses as well as MEDUSA and BiSSE birth-death likelihood models of diversification, to evaluate the evolutionary patterns of lineage accumulation in Lupinus. We identified 3 significant shifts to increased rates of net diversification (r) relative to background levels in the genus (r = 0.18-0.48 lineages/myr). The primary shift occurred approximately 4.6 Ma (r = 0.48-1.76) in the montane regions of western North America, followed by a secondary shift approximately 2.7 Ma (r = 0.89-3.33) associated with range expansion and diversification of allopatrically distributed sister clades in the Mexican highlands and Andes. We also recovered evidence for a third independent shift approximately 6.5 Ma at the base of a lower elevation eastern South American grassland and campo rupestre clade (r = 0.36-1.33). Bayesian ancestral state reconstructions and BiSSE likelihood analyses of correlated diversification indicated that increased rates of speciation are strongly associated with the derived evolution of perennial life history and invasion of montane ecosystems. Although we currently lack hard evidence for "replicate adaptive radiations" in the sense of convergent morphological and ecological trajectories among species in different clades, these results are consistent with the hypothesis that iteroparity functioned as an adaptive key innovation, providing a mechanism for range expansion and rapid divergence in upper elevation regions across much of the New World.

Adaptive radiation, correlated and contingent evolution, and net species diversification in Bromeliaceae

“…Such predictions, when combined with differences among clades in dispersalability and thus the tendency to speciate, can help explain the overall diversity of innovations, species, ecological zones, and geographic areas invaded, summed across radiations. Moore and Donoghue (2007) and Drummond et al (2012b) addressed similar questions involving two families of Dipsacales and for Lupinus. Both studies identified invasion of extensive cordilleras as a major determinant of diversification, but failed to recognize the cumulative contribution of different radiations to overall diversity even when diversification showed no acceleration in any particular radiation, failed to identify key innovations that might underlie the invasion of different regions and ecological zones, and failed to recognize the importance of shared key landscapes (e.g., recently uplifted, extensive cordilleras) that could themselves trigger multiple radiations (Givnish, 1997).…”

Legume Crops Phylogeny and Genetic Diversity for Science and Breeding

“…The Genisteae tribe is currently considered to include 618 species in 25 genera (Cardoso et al, 2013), and its diversity is centered in the Mediterranean region and in the Canary Islands (Cristofolini, 1997; Cristofolini and Chiapella, 1984). Lupinus is the largest Genisteae genus, comprising 267 species, and appears to be monophyletic in origin (Ainouche and Bayer, 1999;Drummond et al, 2012). Chromosome numbers range between 2n = 24 to 2n = 52, and there are multiple lines of evidence showing that at least one polyploidy event has taken place since the divergence of Genisteae from other Papilionoid legumes (Wolko and Weeden, 1989;Gupta et al, 1996;Naganowska et al, 2003;Nelson et al, 2006;Parra-Gonzalez et al, 2012;Yang et al, 2013b;Kroc et al, 2014).…”

“…Lupinus in the Andes has among the highest known rates of species diversification for any angiosperm genus (Hughes and Eastwood, 2006). The vast range of morphological variation (from tiny herbs to large trees) and ecological adaptation (from coastal sand dunes to montane forests) pose challenges for resolving phylogenetic relationships using taxonomic methods (Drummond et al, 2012). Comparisons of nuclear and chloroplast DNA sequences (Ainouche and Bayer, 1999;Wink and Mohamed, 2003;Ainouche et al, 2004;Ree et al, 2004;Drummond and Hamilton, 2007;Drummond, 2008;Eastwood et al, 2008b;Drummond et al, 2012) have made some progress toward resolving Lupinus phylogeny, but ambiguities still remain.…”

Accelerated diversification is related to life history and locomotion in a hyperdiverse lineage of microbial eukaryotes (Diatoms, Bacillariophyta)

“…Numerous life history traits have been linked to net diversification (birth − death, r  =  b  −  d ) in vascular plants. These include features associated with longevity (annual vs perennial, Drummond et al ., 2012), seed dispersal (Leslie et al ., 2013; Beaulieu & O'Meara, 2016) and mechanisms that promote outcrossing, such as self‐incompatibility (Goldberg et al ., 2010) and heterostyly (de Vos et al ., 2014). Similar patterns are also evident in animals.…”