How common is ecological speciation in plant-feeding insects? A 'Higher' Nematinae perspective.
BACKGROUND
Ecological speciation is a process in which a transiently resource-polymorphic species divides into two specialized sister lineages as a result of divergent selection pressures caused by the use of multiple niches or environments. Ecology-based speciation has been studied intensively in plant-feeding insects, in which both sympatric and allopatric shifts onto novel host plants could speed up diversification. However, while numerous examples of species pairs likely to have originated by resource shifts have been found, the overall importance of ecological speciation in relation to other, non-ecological speciation modes remains unknown. Here, we apply phylogenetic information on sawflies belonging to the 'Higher' Nematinae (Hymenoptera: Tenthredinidae) to infer the frequency of niche shifts in relation to speciation events.


RESULTS
Phylogenetic trees reconstructed on the basis of DNA sequence data show that the diversification of higher nematines has involved frequent shifts in larval feeding habits and in the use of plant taxa. However, the inferred number of resource shifts is considerably lower than the number of past speciation events, indicating that the majority of divergences have occurred by non-ecological allopatric speciation; based on a time-corrected analysis of sister species, we estimate that a maximum of c. 20% of lineage splits have been triggered by a change in resource use. In addition, we find that postspeciational changes in geographic distributions have led to broad sympatry in many species having identical host-plant ranges.


CONCLUSIONS
Our analysis indicates that the importance of niche shifts for the diversification of herbivorous insects is at present implicitly and explicitly overestimated. In the case of the Higher Nematinae, employing a time correction for sister-species comparisons lowered the proportion of apparent ecology-based speciation events from c. 50-60% to around 20%, but such corrections are still lacking in other herbivore groups. The observed convergent but asynchronous shifting among dominant northern plant taxa in many higher-nematine clades, in combination with the broad overlaps in the geographic distributions of numerous nematine species occupying near-identical niches, indicates that host-plant shifts and herbivore community assembly are largely unconstrained by direct or indirect competition among species. More phylogeny-based studies on connections between niche diversification and speciation are needed across many insect taxa, especially in groups that exhibit few host shifts in relation to speciation.
Nyman
Tommi
T
Department of Biology, University of Eastern Finland, PO Box 111, FI-80101 Joensuu, Finland. Tommi.Nyman@uef.fi
Vikberg
Veli
V
Smith
David R
DR
Boevé
Jean-Luc
JL
D000818:Animals; D004463:Ecology; D007313:Insecta / Q000145:classification* / Q000235:genetics; D010802:Phylogeny; D010944:Plants / Q000469:parasitology*; D013045:Species Specificity
J Evol Biol. 2006 Jul;19(4):1314-26
16780532
Evolution. 2009 Oct;63(10):2595-610
19500148
Mol Phylogenet Evol. 2009 Apr;51(1):94-9
18588992
Proc Natl Acad Sci U S A. 2001 May 22;98(11):6221-6
11353840
Nature. 2008 Jan 17;451(7176):279-83
18202643
Trends Ecol Evol. 2009 Jul;24(7):394-9
19409647
Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3071-81
18579479
BMC Biol. 2007 Jan 26;5:3
17257412
Evolution. 2006 Dec;60(12):2604-21
17263120
Syst Biol. 2008 Oct;57(5):758-71
18853362
BMC Evol Biol. 2006 Jan 18;6:4
16420707
Proc Natl Acad Sci U S A. 2009 Jun 16;106 Suppl 1:9955-62
19528639
BMC Evol Biol. 2009 Nov 27;9:273
19941669
Trends Ecol Evol. 2007 Jun;22(6):298-307
17324485
Science. 2007 Dec 21;318(5858):1913-6
18096805
Syst Biol. 2004 Feb;53(1):120-7
14965907
Evolution. 2000 Apr;54(2):526-33
10937229
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18103-8
19805134
Proc Natl Acad Sci U S A. 2006 Jul 18;103(29):10947-51
16818884
BMC Evol Biol. 2009 Nov 21;9:268
19930590
Evolution. 2006 Nov;60(11):2311-28
17236423
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18054-61
19815508
Nature. 2007 Aug 9;448(7154):696-9
17687325
Trends Ecol Evol. 2001 Jul 1;16(7):391-399
11403872
Proc Biol Sci. 2010 Oct 22;277(1697):3131-8
20504811
Am Nat. 2000 Apr;155(4):419-434
10753072
Ecol Lett. 2007 Oct;10(10):977-94
17855811
Proc Natl Acad Sci U S A. 2009 May 5;106(18):7495-500
19380742
Mol Ecol. 2009 Nov;18(21):4450-62
19793353
Science. 2007 Mar 9;315(5817):1420-3
17347442
Am J Bot. 2000 Jan;87(1):67-75
10636831
Philos Trans R Soc Lond B Biol Sci. 2002 Apr 29;357(1420):471-92
12028786
BMC Evol Biol. 2007 Nov 08;7:214
17996036
Proc Natl Acad Sci U S A. 2009 Apr 28;106(17):7083-8
19365072
Evolution. 2006 Aug;60(8):1622-37
17017063
Science. 2000 Jun 30;288(5475):2349-50
10875916
Bioinformatics. 1998;14(9):817-8
9918953
Proc Natl Acad Sci U S A. 2009 Oct 27;106(43):18062-6
19706441
Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3209-13
16492742
Ecol Lett. 2009 Aug;12(8):735-43
19558515
Bioinformatics. 2003 Aug 12;19(12):1572-4
12912839
Trends Ecol Evol. 2009 Mar;24(3):145-56
19185951
Science. 1999 Aug 20;285(5431):1265-7
10455053
Trends Ecol Evol. 2008 Nov;23(11):619-30
18823678
Syst Biol. 1997 Dec;46(4):722-47
11975339
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13875-9
19667210
Evolution. 1998 Dec;52(6):1744-1759
28565322
Trends Ecol Evol. 2001 Jul 1;16(7):381-390
11403871
BMC Biol. 2007 Nov 01;5:49
17976232
Ecol Lett. 2008 Jun;11(6):624-36
18384363
Biol Rev Camb Philos Soc. 2010 May;85(2):393-411
20002390
Evolution. 2007 Jul;61(7):1641-60
17598746
Proc Natl Acad Sci U S A. 1999 Jul 6;96(14):8013-6
10393939
Evolution. 2001 Dec;55(12):2503-22
11831666
Evolution. 1997 Dec;51(6):1699-1711
28565128
Nature. 2006 May 11;441(7090):210-3
16467788